GIFT   OF 


BiOLOGY 

UBRARY 

G 


-   MORPHOLOO¥--: 
OF    ANGIOSPERMS 


(MORPHOLOGY  OF  SPEKMATOPHYTES.     PART  II) 


BY 


JOHN    MERLE   COULTER,   PH.  D. 

BOTANY,  THE    UNIVERSITY    OF   CHICAGO 


HEAD    OF    DEPARTMENT    OF 


AND 


CHARLES  JOSEPH   CHAMBERLAIN,   PH.  D. 

INSTRUCTOR   IN    KOTANY,    THE    UNIVERSITY    OF    CHICAGO 


ILLUSTRATED 


NEW    YORK 

D.    APPLETON     AND     COMPANY 
1903 


•          ' 
G 


COPYRIGHT,   1903 
BY    D.    APPLETON    AND    COMPANY 


Published  July,   1903 


PEEFACE 


Ix  1901  we  published  the  first  part  of  a  work  entitled 
Morphology  of  Spermatophytes,  containing  an  account  of  the 
Gymnosperms.  At  that  time  it  was  our  purpose  to  issue  as 
a  second  part  an  account  of  the  Angiosperms,  which  would  also 
contain  a  complete  index  of  the  whole  work.  We  have  become 
convinced,  however,  that  such  an  association  of  these  two  great 
groups  would  help  to  emphasize  a  relationship  that  does  not 
exist,  and  that  Gymnosperms  and  Angiosperms  should  be 
treated  as  independent  groups,  coordinate  with  Pteridophytes. 
Therefore,  the  present  volume  is  issued,  not  as  Part  II  of 
Morphology  of  Spermatophyies,  but  as  an  independent  volume 
entitled  Morphology  of  Angiosperms:,  and  any  subsequent 
edition  of  the  previous  volume  will  be  entitled  Morphology  of 
Gymnosperms. 

This  volume,  as  the  preceding,  has  grown  out  of  a  course 
of  lectures  accompanied  by  laboratory  work,  given  for  several 
successive  years  to  classes  of  graduate  students,  preparing  for 
research.  -It  seeks  to  organize  the  vast  amount  of  scattered 
material  so  that  it  may  be  available  in  compact  and  related 
form.  While  careful  attention  has  been  given  to  citations,  so 
that  the  student  may  know  the  groups  that  have  been  inves- 
tigated, and  be  put  in  touch  with  the  original  papers,  the  work 
is  in  no  sense  a  compilation.  The  ground  has  been  traversed 
repeatedly,  for  several  years,  by  various  members  of  the  botan- 
ical staff  and  by  numerous  students,  and  their  results  have 
served  to  check  current  statements,  as  well  as  to  contribute  no 
small  amount  of  new  material. 


Vi  MORPHOLOGY  OF  ANGIOSPERMS 

Any  one  who  has  attempted  to  review  the  literature  of  the 
morphology  of  Angiosperms  will  appreciate  the  great  amount 
of  labor  it  involves,  as  well  as  the  chaotic  condition  of  termi- 
nology and  citations.  There  is  nothing  more  baffling  than  the 
attempt  to  follow  the  guidance  of  the  meager,  indefinite,  and 
often  incorrect  citations  of  the  standard  texts.  It  is  believed, 
therefore,  that  the  attempt  to  reduce  the  numerous  contribu- 
tions to  a  consistent  terminology  and  to  make  the  citations 
fairly  representative  of  the  subject  as  well  as  definite  and  accu- 
rate will  be  of  some  real  service  to  students  of  morphology. 
The  volume,  therefore,  seeks  to  give  to  the  advanced  student  a 
continuous  account  of  the  structures  involved,  and  to  the  research 
student  the  details  of  groups  and  bibliography  that  he  needs. 

In  every  case  where  figures  have  been  copied,  acknowledg- 
ment is  made  and  a  reference  is  given  to  the  original  paper 
containing  the  illustration.  It  should  be  noted  that  much  in- 
formation included  in  the  legends  does  not  appear  in  the  text, 
so  that  in  any  thorough  reading  of  the  book  the  legends  should 
be  included.  The  bibliography  pertaining  to  each  subject  is 
printed  in  chronological  order  at  the  end  of  each  chapter  con- 
taining numerous  citations.  At  the  close  of  the  volume  all  of 
the  cited  bibliography  is  brought  together,  arranged  alphabet- 
ically by  authors. 

It  would  be  too  large  a  task  to  include  a  complete  bibliog- 
raphy of  such  a  subject,  but  we  have  presented  what  may  be 
regarded  as  a  full  representative  bibliography,  containing,  so 
far  as  we  know,  all  of  the  most  important  contributions.  In 
the  very  nature  of  things,  some  citations  may  have  been 
omitted  that  should  have  been  included,  but  there  has  been 
no  intentional  neglect. 

~No  attempt  is  made  to  present  the  details  of  floral  structure, 
so  fully  described  by  the  earlier  morphologists  and  taxonomists, 
since  they  are  easily  accessible  in  numerous  texts.  Xor  have 
we  ventured  to  enter  the  old  and  extensive  field  of  anatomy, 
although  many  of  its  details  are  pertinent  to  morphology.  In 


PREFACE  vii 

its  later  development,  however,  it  has  contributed  so  many 
important  data  essential  in  any  discussion  of  phylogeny  that 
we  have  asked  Professor  E.  C.  Jeffrey  to  present  the  general 
outlines  of  the  subject  in  the  last  two  chapters  of  this  volume, 
a  discussion  which  includes  both  Gymnosperms  and  Angio- 
sperms.  It  is  hoped  that  this  presentation  will  help  to  stimu- 
late the  cultivation  of  an  important  field  of  research  too  much 
neglected  in  this  country. 

It  did  not  seem  necessary  to  treat  the  two  great  groups  of 
Angiosperms  separately.  They  are  so  similar  in  their  essential 
morphological  features  that  their  separate  presentation  would 
have  involved  a  needless  amount  of  repetition.  We  have  also 
continued  to  regard  the  spore  mother-cell  as  the  end  of  the 
sporophytic  generation,  and  its  division  as  the  beginning  of  the 
gametophyte.  The  reasons  for  this  are  more  fully  presented 
in  the  present  volume  than  in  the  preceding. 

In  the  chapters  upon  classification  we  have  presented  the 
scheme  elaborated  by  Professor  Engler,  believing  that  it  is 
the  best  expression  of  current  knowledge  of  relationship  ap- 
plied to  the  whole  group,  and  that  it  is  suggestive  of  the  most 
critical  regions  for  research.  This  has  not  been  pressed  to  the 
dreary  details  of  minor  groups,  for  these  are  easily  accessible. 
It  has  rather  been  our  intention  to  present  the  general  ideas 
involved  in  the  alliances  of  first  rank,  so  that  principles  rather 
than  details  may  be  prominent.  We  have  also  thought  that 
the  special  student  should  be  somewhat  familiar  with  the  his- 
tory of  the  group,  so  far  as  known,  its  geographic  distribution, 
and  the  current  notions  as  to  its  phylogeny.  The  last  subject 
may  be  regarded  as  more  theoretical  than  profitable,  but  the 
final  aim  of  morphology  is  a  definite  phylogeny,  and  advance 
toward  it  must  be  made  by  a  succession  of  theoretical  con- 
clusions. 

JOHX    M.     COULTEE. 

CHAELES  J. 

THE  UNIVERSITY  OF  CHICAGO, 
January,  1903. 


CONTENTS 


CHAPTER  PAGE 

I. — INTRODUCTORY 1 

Angiosperras  and  Gymnosperms  contrasted,  1 — Sperraatophytes 
not  a  natural  group,  3 — Monocotyledons  and  Dicotyledons  con- 
trasted, 4. 

II.— THE  FLOWER 8 

Definition  of  a  flower,  9 — Origin  of  floral  leaves,  9 — Tendencies 
in  the  evolution  of  the  flower,  10 — Organogeny  of  the  flower,  16 
— Dioecism,  20 — Morphology  of  floral  members,  22 — Stamen,  23 
—Carpel,  24. 

III. — THE  MICROSPORAXGIUM 27 

Origin  from  periblem,  27 — Cauline  microsporangia,  28 — Number 
of  microsporangia,  29 — Time  of  formation,  30 — Development. 
32 — Archesporium,  32 — Parietal  layers,  34 — Tapetum,  36 — 
Mother-cells,  38 — Dehiscence,  41 — Line  of  demarcation  between 
sporophyte  and  gametophyte,  41. 

IV. — THE  MEGASPORAXGIUM 46 

Origin  from  periblem,  46 — Cauline  ovules,  46— Foliar  ovules.  50 
— Morphological  nature  of  ovule,  51 — Time  of  development  of 
megasporangia,  52 — Development  of  ovule,  53 — Archesporium, 
57— Parietal  cells,  62— Mother-cell,  66. 

V. — THE  FEMALE  GAMETOPHYTE 71 

The  tetrad,  71 — Number  of  megaspores,  76 — Reduction  of  chro- 
mosomes, 80 — The  functioning  megaspore,  84 — Number  of  em- 
bryo-sacs, 86 — Germination  of  megaspore,  87 — Variations  in 
history,  89— Egg-apparatus.  93 — Synergids,  94 — Fusion  of  polar 
nuclei,  95 — Antipodal  cells,  96— Enlargement  of  embryo-sac,  103 
— The  nutritive  jacket,  103 — Haustoria,  104 — The  mechanism 
for  nutrition,  108. 

VI. — THE  MALE  GAMETOPHYTE 121 

The  tetrad,  121 — Number  of  microspores,  125 — The  nuclear  divi- 
sions of  the  pollen  mother-cell,  126 — The  microspores,  131 — Ger- 
mination of  microspore,  132 — Division  of  generative  cell,  135 — 
The  male  nuclei,  136. 

ix 


x  MORPHOLOGY  OF  ANGIOSPERMS 

CHAPTER  PAGE 

VII. — FERTILIZATION 143 

Historical  resume,  143 — Development  of  pollen-tube,  146 — Chala- 
zogamy,  149 — The  pollen-tube  within  the  embryo-sac,  151 — Dis- 
charge of  pollen-tube,  152 — Fusion  of  male  and  female  nuclei, 
153 — Centrosomes,  153 — Double  fertilization,  155 — Male  cell  and 
male  nucleus,  160. 

VIII.— THE  ENDOSPERM .        .        .165 

Contrast  between  Gymnosperms  and  Angiosperms,  165 — The 
fusion  nucleus,  166 — Endosperm  without  fusion,  166 — Endo- 
sperm and  pollination,  167 — Division  of  fusion  nucleus,  169 — 
Two  methods  of  endosperm-formation,  171 — Function  of  endo- 
sperm, 179 — Xenia,  179 — Morphological  character,  181 — Nature 
of  triple  fusion,  182. 

IX.— THE  EMBRYO • 187 

Monocotyledons,  188— Alisma  type,  188— Pistia  type,  192— 
Lilium  type,  193— Orchid  type,  194— Dicotyledons,  196— Cap- 
sella  type,  199— Other  types,  200 — Degree  of  development,  205 
— "  Pseudo-monocotyledons,"  206 — Phylogeny  of  the  cotyledon, 
208 — Parthenogenesis,  210 — Polyembryony,  213. 

X. — CLASSIFICATION  OF  MONOCOTYLEDONS 227 

Spiral  series,  228— Cyclic  series,  234. 

XI. — CLASSIFICATION  of  ARCHICHLAMYDEAE 240 

XII. — CLASSIFICATION  OF  SYMPETALAE 252 

XIII. — GEOGRAPHIC  DISTRIBUTION  OF  ANGIOSPERMS 261 

Monocotyledons,  262 — Archichlamydeae,  266 — Sympetalae,  268. 

XIV.— FOSSIL  ANGIOSPERMS 272 

Monocotyledons,  272 — Dicotyledons,  276. 

XV. — PHYLOGENY  OF  ANGIOSPERMS 280 

Are  Angiosperms  monophyletic  I  280 — Relation  to  Gymno- 
sperms, 283 — Relation  to  Pteridophytes,  285 — Theories  of  alter- 
nation of  generations,  288— Theory  of  the  strobilus,  288— The 
mutation  theory,  292. 

XVI. — COMPARATIVE  ANATOMY  OF  THE  GYMNOSPERMS  AND  THEIR  ALLIES    296 
Pteridophytes,  296— Cycadofilices,  300— Cycadales,  304— Ben- 
nettitales,  306— Cordaitales,  307— Ginkgoales,  307— Coniferales, 
308— Gnetales,  310. 

XVII. — COMPARATIVE  ANATOMY  OF  ANGIOSPERMS 311 

Dicotyledons,  311 — Monocotyledons,  314. 


MORPHOLOGY  OF  ANGIOSPERMS 


CHAPTER    I 

INTBODUCTOBY 

THERE  is  a  very  large  element  of  uncertainty  in  a  presenta- 
tion of  the  special  morphology  of  Angiosperms,  chiefly  because 
of  the  vast  amount  of  unstudied  material,  but  also  because  of 
the  inequality  in  the  accuracy  and  definiteness  of  the  work 
done.  However,  the  general  outlines  seem  to  be  fairly  well 
established,  and  their  filling  in  must  long  occupy  morphologists. 

Although  two  very  distinct  groups  of  Angiosperms  are 
recognized,  the  Monocotyledons  and  the  Dicotyledons,  their  es- 
sential morphology  is  so  similar  that  separate  treatment  would 
involve  needless  repetition.  The  chief  differences  between  them 
have  to  do  with  the  structure  of  the  vegetative  body  of  the 
sporophyte.  A  general  treatment  of  these  differences  is  not 
necessary  in  a  book  dealing  with  special  morphology,  for  it 
belongs  to  elementary  instruction;  while  a  special  treatment 
would  lead  into  the  immense  field  of  anatomy,  which  it  is  not 
the  purpose  of  this  book  to  present.  So  far  as  anatomical 
studies  have  a  conspicuous  bearing  upon  the  phylogeny  of  the 
great  groups,  they  are  presented  by  Professor  E.  C.  Jeffrey 
in  the  last  two  chapters. 

In  contrasting  Angiosperms  with  Gymnosperms,  one  is  im- 
->-d  by  the  fact  that  a  group  of  plants  comprising  more 
than  one  hundred  thousand  known  species  can  not  be  presented 
with  the  same  confidence  and  detail  as  can  a  group  represented 
by  a  scant  four  hundred  species.  And  yet,  what  have  been 
agreed  upon  as  the  essential  morphological  features  of  these 
groups  appear  to  be  more  uniform  in  Angiosperms  than  in 
Gymnosperms.  In  our  treatment  of  the  latter  group,  the  great 

1 


MORPHOLOGY   OF  AXGIOSPERMS 

wer-e  ^presented  separately  because  of  the  diversities; 
e  morphological  diversities  among  Angiosperms  seem  to 
be  not  so  much  those  of  groups  as  of  habit  and  habitat.  While 
it  is  generally  agreed  that  the  seed-bearing  habit  was  devel- 
oped independently  in  more  than  one  phylum,  and  that  the 
Gymnosperms  and  Angiosperms  have  probably  no  immediate 
phylogenetic  relation  to  one  another,  it  is  of  interest  to  note 
the  essential  contrasting  features  of  the  two  great  seed-bearing 
groups. 

The  chief  contrast  in  the  sporophyte  is  that  in  Gymno- 
sperms pollination  results  in  bringing  the  pollen  in  contact 
with  the  ovule,  while  in  Angiosperms  the  result  of  pollination 
places  the  pollen  in  contact  with  a  receptive  surface  developed 
by  the  carpel.  This  contrast  involves  great  differences  in  mor- 
phological structure,  so  great,  in  fact,  that  it  is  hard  to  imagine 
one  of  these  conditions  as  having  been  derived  from  the  other. 
The  method  of  pollination  might  also  be  mentioned  as  a  con- 
trasting feature,  since  the  primitive  anemophilous  habit  seems 
to  be  universal  among  the  Gymnosperms,  while  among  Angio- 
sperms it  prevails  only  among  those  groups  that  may  be  re- 
garded as  primitive.  There  accompanies  this  contrast  a  similar 
one  in  connection  with  the  flower.  Just  how  this  structure 
may  be  defined  is  considered  in  the  next  chapter,  but  the  char- 
acteristic flowers  of  Angiosperms  have  no  representative  among 
Gymnosperms,  however  much  the  older  morphology  felt  com- 
pelled to  homologize  them.  However,  the  method  of  pollination 
and  the  flower  are  but  corollaries  to  the  fundamental  contrast 
involved  in  the  contact  of  the  pollen  with  the  ovule  in  the  one 
case,  and  with  the  carpel  in  the  other. 

A  second  fundamental  distinction  in  connection  with  the 
sporophyte  is  to  be  found  in  the  embryogeny  of  the  two  groups. 
In  the  Gymnosperms,  the  free  nuclear  division  within  the  fer- 
tilized egg,  and  the  use  of  the  bulk  of  the  egg  as  a  food  re- 
serve in  most  forms  are  in  sharp  contrast  with  the  absence  of 
free  nuclear  division  in  the  Angiosperm  egg,  a  character  ap- 
pearing, however,  in  Gnetum  and  Tumboa. 

If  the  contrast  between  the  sporophytes  of  Gymnosperms 
and  Angiosperms  be  pressed  into  anatomical  details,  the  differ- 
ences are  found  to  be  quite  as  striking,  though  perhaps  a  little 
more  perplexing. 


INTRODUCTORY  3 

The  contrast  between  the  gametophytes  of  the  two  groups, 
especially  the  female  gametophytes,  is  even  greater  than  that 
shown  by  the  sporophytes.  The  male  gametophytes  of  Gymno- 
sperins  when  contrasted  with  those  of  heterosporous  Pterid- 
ophytes  present  a  much  shorter  history;  and  the  gametophytic 
structure  produced  by  the  Gymnosperm  microspore  involves 
the  formation  of  two  or  three  times  as  many  cells  as  are  formed 
in  the  germination  of  the  Angiosperm  microspore.  The  female 
gametophytes  of  the  two  groups,  however,  are  in  the  main  stri- 
kingly different.  As  is  well  known,  the  female  gametophytes 
of  Gymnosperrns  in  general,  with  their  well-organized  tissue 
and  archegonia,  are  almost  the  exact  counterparts  of  those  of 
Selaginella  and  Isoetes;  while  the  female  gametophyte  of  An- 
gio perms  remains  a  morphological  puzzle,  made  still  more 
perplexing  by  the  discovery  of  the  wide-spread  phenomenon 
styled  "  double  fertilisation!"  It  is  a  very  significant  fact,  how- 
ever, that  in  spite  of  the  difficulties  of  the  female  gametophyte 
of  Angiosperms  in  the  way  of  interpretation  and  of  origin,  it 
is  one  of  the  most  remarkably  consistent  structures  known  to 
morphology,  the  sequence  of  events  in  its  history  representing 
an  almost  unvarying  schedule,  and  supplying  one  of  the  strong- 
est arguments  in  favor  of  the  monophyletic  origin  of  Angio- 
sperms. 

In  view  of  these  and  other  differences  between  Angiosperms 
and  Gymnosperms,  the  question  is  raised  whether  we  have  not 
been  too  narrow  in  the  conception  of  the  seed-bearing  habit  in 
compelling  these  two  groups  to  remain  as  subdivisions  of  a 
group  Spermatophytes  coordinate  with  Pteridophytes  and 
Bryophytes.  In  a  certain  sense,  to  select  a  single  character, 
such  as  seed-bearing,  as  a  basis  for  the  union  of  two  groups 
otherwise  dissimilar  is  suggestive  of  artificial  classification. 
Furthermore,  to  separate  the  female  gametophytes  of  Gymno- 
sperms from  those  of  the  heterosporous  Lycopodiales,  and  to 
•iate  them  with  those  of  Angiosperms,  is  certainly  to  do 
violence  to  a  most  important  suggestion  of  natural  relation- 
ships. In  our  judgment,  therefore,  the  designation  Sperma- 
tophytes should  be  used  in  a  general  way,  as  a  term  of  con- 
venience rather  than  of  classification,  only  less  extensive  in  its 
application  than  "  vascular  plants " ;  and  Gymnosperms  and 
Angiosperms  should  be  recognized  as  two  groups  coordinate 


4  MORPHOLOGY  OF  ANGIOSPERMS 

with  Pteridophytes  and  Bryophytes.  In  fact,  Pteridophytes 
and  Gymnosperms  together  form  a  much  more  natural  group 
than  do  Gymnosperms  and  Angiosperms ;  and  this  fact  should 
be  emphasized  by  treating  Gymnosperms  and  Angiosperms  as 
groups  of  the  first  rank. 

Although  it  is  a  question  whether  Gymnosperms  and  An- 
giosperms should  be  so  closely  associated  as  to  form  the  two 
subdivisions  of  a  great  group,  there  can  be  no  question  that 
Monocotyledons  and  Dicotyledons  are  naturally  and  intimately 
associated.  This  proposition  is  not  affected  by  the  question  of 
their  common  origin,  but  is  based  upon  their  essential  mor- 
phological features,  whatever  may  have  been  their  origin.  The 
characters  that  separate  Monocotyledons  and  Dicotyledons  are 
cumulative  rather  than  specific,  and  although  the  character  of 
the  embryo  is  held  to  be  the  decisive  one  in  every  case,  there  is 
danger  of  using  it  with  unnatural  rigidity.  When  a  decision 
between  two  groups  is  reduced  to  a  single  character,  there  is  a 
suspicion  either  that  the  groups  can  only  be  separated  arti- 
ficially or  that  too  much  stress  is  laid  upon  the  character.  Mon- 
ocotyledons and  Dicotyledons  are  best  distinguished  by  cer- 
tain tendencies  that  involve  several  characters,  and  if  these 
tendencies  are  supported  by  the  character  of  the  embryo  the 
case  is  clear.  A  brief  statement  of  the  conspicuous  differences 
may  be  of  service. 

1.  In  the  embryo  of  Monocotyledons  the  cotyledon  is  ter- 
minal and  the  stem  tip  lateral  in  origin ;  while  in  Dicotyledons 
the  stem  tip  is  terminal  and  the  cotyledons  lateral  in  origin. 
This  character  seems  to  be  fundamental,  and  at  the  present  time 
is  the  only  one  that  may  be  regarded  as  decisive.      That  the 
difference    indicated   will    always   be   expressed    in   the    above 
terms  is  not  likely,  for  the  nature  of  the  cotyledon  is  in  ques- 
tion, and  the  significance  of  this  relation  of  parts  has  yet  to  be 
determined. 

2.  The  development  of  the  vascular  bundles  in  the  stele  is 
very  different  in  the  two  groups.     This  difference  involves  not 
only  the  arrangement  of  the  bundles,  but  also  the  presence  or 
absence  of  fascicular  cambium,  and  is  far-reaching  in  its  re- 
sults upon  the  habit  of  the  body.     In  the  case  of  perennial 
stems  it  involves  the  general  ability  to  increase  in  diameter, 
arrd  this  affects  the  powTer  of  branching,  and  this  in  turn  deter- 


INTRODUCTORY  5 

mines  the  question  of  an  annual  increase  in  the  display  of 
foliage,  which  means  the  working  power  of  the  body.  This 
character  can  not  be  used  as  a  specific  test  for  the  two  groups ; 
nor  must  it  be  pressed  in  certain  features  alone  or  too  rigidly. 
When  intelligently  applied,  it  is  probably  only  second  in  im- 
portance to  the  character  supplied  by  the  embryo;  but  it  must 
be  remembered  that  these  prevailing  tendencies  of  the  two 
groups  are  in  some  instances  exchanged. 

3.  The  characteristic  foliage  leaves  of  Monocotyledons  have 
a  closed  venation,  while  in  Dicotyledons  the  venation  is  open. 
This  character  involves  many  differences  in  detail.  For  ex- 
ample, as  a  result  the  Monocotyledon  leaf  is  entire,  while  the 
Dicotyledon  leaf,  with  veins  ending  freely  in  the  margin,  is 
inclined  to  branch  more  or  less,  this  tendency  expressing  itself 
in  the  greatest  variety  of  ways  from  simple  teeth  to  the  so- 
called  "  compound  leaves."  *  It  is  also  true  in  general  that  in 
Monocotyledons  there  is  a  sharp  contrast  in  size  between  the 
principal  veins  of  the  leaf  and  the  reticulating  veinlets;  while 
in  Dicotyledons  the  gradation  is  so  gradual  that  the  reticulation 
becomes  very  evident.  It  may  be  well  to  call  attention  to  the 
fact  that  while  the  so-called  "  parallel "  venation  may  be  of 
service  in  distinguishing  the  majority  of  Monocotyledons  in 
temperate  regions,  as  contrasted  with  the  "pinnate"  or  "pal- 
mate "  venation  of  Dicotyledons,  it  loses  its  significance  when 
the  tropical  Monocotyledons  are  included.  The  distinctive 
character  of  closed  or  open  venation  can  not  be  applied  to  all 
Monocotyledons  and  Dicotyledons,  and  is  certainly  less  gen- 
eral in  its  application  than  the  two  characters  already  given. 
As  a  character  to  be  used  in  a  cumulative  way,  however,  it 
deserves  prominent  mention. 

•i.  Among  Monocotyledons  and  Dicotyledons  with  cyclic 
flowers  the  establishment  of  three  as  the  cycle  number  of  the 
former,  and  of  five  or  four  as  the  cycle  number  of  the  latter 
is  quite  distinctive.  In  fact,  the  constancy  with  which  these 
numbers  appear  is  more  remarkable  than  the  exceptions.  Of 
necessity,  this  character  is  of  comparatively  limited  use,  but 
it  is  of  service  among  the  cyclic  families,  and  also  among  those 
families  some  of  whose  floral  parts  are  in  cycles.  The  persist- 

*  This  term  should  be  abandoned  for  leaves,  as  has  the  term  "compound 
flower  "  for  the  characteristic  head  of  Compositae. 


6  MORPHOLOGY  OF  ANGIOSPERMS 

ent  tendency  of  the  spiral  groups  of  Monocotyledons  and  Dicot- 
yledons to  express  the  appropriate  cyclic  number,  when  the 
conditions  seem  to  favor  indefinite  numbers,  is  even  more  re- 
markable than  the  constant  reappearance  of  the  cyclic  number 
in  families  in  which  it  has  become  established.  Just  what  has 
determined  these  numbers  for  the  two  great  groups  is  an  inter- 
esting but  unanswered  question.  The  problem  is  confused  by 
the  fact  that  certain  plants,  undoubtedly  Monocotyledons  or 
Dicotyledons  by  all  the  usual  tests,  have  the  cycle  number  of 
the  other  group. 

In  addition  to  the  distinguishing  characters  enumerated 
above,  others  of  much  less  general  application  have  been  sug- 
gested, but  it  is  not  clear  that  any  of  them  are  really  significant 
group  characters. 

There  are  certain  general  differences  in  the  leaves  of  the 
two  groups  that  deserve  mention,  since  they  come  as  near  rep- 
resenting group  tendencies  as  any  of  the  secondary  characters 
just  enumerated.  Among  Dicotyledons  the  foliage  leaf  is  gen- 
erally more  differentiated  than  among  Monocotyledons,  inclu- 
ding a  petiole  and  often  stipules.  In  fact  stipules  would  be 
quite  characteristic  of  Dicotyledons  were  they  not  lacking  in 
so  many,  for  Monocotyledons  possess  no  such  structures. 
Among  the  latter,  however,  there  is  the  almost  equally  char- 
acteristic leaf-sheath  from  which  the  blade  directly  arises. 
This  general  distinction  between  the  leaves  of  the  two  groups 
must  have  some  unappreciated  significance,  and  suggests  that 
it  may  represent  something  as  fundamental  as  do  the  differ- 
ences in  the  embryo  and  the  stele. 

The  so-called  a  germination  "  of  the  seed  is  suggestive  of 
different  tendencies  in  the  two  groups,  but  the  data  seem  to 
be  too  scanty  and  indefinite  as  yet  for  safe  generalization.  So 
far  as  they  do  exist,  they  indicate  a  tendency  in  Monocotyledons 
to  free  the  stem  and  root  tips  by  the  elongation  of  a  portion 
of  the  cotyledon,  the  other  portion  remaining  in  contact  with 
the  endosperm  as  a  digesting  and  absorbing  organ,  very  sug- 
gestive of  the  "  foot "  of  Pteridophytes ;  while  in  Dicotyledons 
the  tendency  is  to  liberate  the  growing  points  and  cotyledons 
by  the  elongation  of  the  hypocotyl,  and  even  hypogean  cotyle- 
dons are  not  related  to  endosperm  as  digestive  and  absorbing 
organs. 


INTRODUCTORY  7 

It  is  claimed  that  the  prophyllum  *  of  Monocotyledons  is 
solitary  and  posterior,  while  in  Dicotyledons  there  are  two  op- 
posite and  lateral  prophylla.  If  such  structures  generally 
occurred,  or  even  if  this  distinction  were  generally  true  when 
they  do  occur,  such  a  character  would  be  significant,  for  the 
prophyllum  certainly  has  a  definite  connection  with  the  position 
of  the  successive  floral  parts  in  relation  to  the  main  axis. 

It  has  been  urged  also  that  the  Monocotyledons  are  char- 
acterized by  a  small  embryo  embedded  in  an  abundant  endo- 
sperm, and  that  in  Dicotyledons  the  tendency  is  to  develop 
larger  embryos  at  the  expense  of  the  endosperm.  This  involves 
so  many  and  such  important  exceptions  that  it  can  hardly  be 
regarded  as  a  distinction  between  these  two  great  groups. 

The  roots  of  Monocotyledons  are  said  to  differ  from  those 
of  Dicotyledons  in  that  the  primary  roots  are  short-lived  and 
there  is  no  persistent  root-system  as  in  many .  Dicotyledons. 
While  this  may  be  true  of  Monocotyledons  in  general,  it  is  also 
true  of  many  Dicotyledons,  and  can  not  be  used  as  a  distinct- 
ive character. 

All  the  characters  enumerated  above,  both  those  of  primary 
and  those  of  secondary  importance,  are  to  be  considered  in  any 
general  characterization  of  the  two  groups;  but  it  must  be  re- 
membered that  most  of  them  await  confirmation  as  essential 
group  characters.  It  is  of  interest  to  note  that  they  are  all 
characters  of  the  vegetative  sporophyte,  and  that  the  sporangia 
and  gametophytes  of  Monocotyledons  and  Dicotyledons  have 
tlius  far  given  no  tangible  evidence  of  group  differences. 

*  Translated  into  German  as  VorUatt,  and  into  English  as  fore-leaf.  The 
first  leaf  on  a  branch,  but  used  only  in  connection  with  the  bractlets  of  a 
flower  cluster. 


CHAPTER    II 

THE    FLOWER 

THE  morphology  of  the  flower  of  Angiosperms  has  an  enor- 
mous literature,  much  of  which  is  now  more  curious  than  valu- 
able. It  is  not  the  purpose  of  this  book  to  present  the  numerous 
details  and  extensive  terminology  that  were  so  conspicuous  a 
feature  of  the  older  morphology,  dominated  as  it  was  by  the 
doctrine  of  metamorphosis.  For  these  the  student  is  referred 
to  Eichler's  Bluthendiagramme  (1875— '78),  in  which  may  be 
found  the  most  complete  account  of  the  flower  of  Angiosperms- 
from  this  standpoint.  The  English  student  will  also  find  an 
admirable  short  account  of  the  same  subject  from  the  same 
standpoint  in  Gray's  Structural  Botany  (1879).  A  presenta- 
tion that  combines  much  of  the  older  method  of  treatment  with 
newer  points  of  view  appears  in  Goebel's  Outlines  of  Classi- 
fication and  Special  Morphology  of  Plants  (English  transla- 
tion, 1887).  Among  the  later  important  literature  the  follow- 
ing may  be  consulted:  Goebel's  Vergleichende  Entwicklungs- 
geschichte  der  Pflanzenorgane  in  Schenck's  Handbuch  der 
Botanik  (3 ':  99-432.  figs.  126.  1884);  Celakovsky's  Ueber 
den  phylogenetischen  Entwicklungsgang  der  Bliite  und  liber 
den  Ursprung  der  Blumenkrone,  I  and  II  (Sitzber.  Konigl. 
Bohm.  Gesell.  Wiss.  1896  and  1900)  ;  Eamiller's  Biogenetische 
Untersuchungen  iiber  verkummerte  oder  mngebildete  Sexualor- 
gane  (Flora  82:  133-168.  figs.  10.  1896)  ;  Engler  and  Prantl's- 
Die  Natiirlichen  Pflanzenf  amilien  ;  .Goebel's  Organographie  der 
Pflanzen  (vol.  ii,  1901).*  These  works  and  others  like  them 
must  be  consulted  for  the  details  of  the  structure  of  angio- 

*  It  should  be  understood  that  in  this  mention  of  the  literature  of  the 
flower  only  certain  important  works  are  cited,  and  that  only  in  the  subse- 
quent chapters  is  there  any  attempt  at  presenting  fairly  complete  lists  of  the 
important  literature. 

8 


THE  FLOWER  9 

spermous  flowers,  for  in  this  chapter  only  certain  of  the  broader 
morphological  features  will  be  discussed. 

Any  strict  definition  of  a  flower  seems  to  be  impossible. 
That  the  morphological  precursor  of  the  angiospermous  flower 
was  some  such  structure  as  the  strobilus  of  Pteridophytes  seems 
reasonably  clear.  In  fact,  the  strobilus  is  plainly  continued 
among  the  Angiosperms  in  spiral  flowers  and  spirally  arranged 
members.  The  appearance  of  distinct  floral  leaves  associated 
with  sporophylls,  however,  is  characteristic  of  the  higher  An- 
giosperms. If  a  flower  is  essentially  a  sporophyll  or  a  set  of 
sporophylls,  as  the  older  definition  insists,  Pteridophytes  must 
be  included  among  flowering  plants.  If,  on  the  other  hand,  a 
flower  is  characterized  by  floral  leaves,  many  Angiosperms  are 
not  flowering  plants.  In  any  event,  the  term  flower  is  of  indefi- 
nite application,  and  is  incapable  of  sharp  definition.  It  is  a 
term  of  convenience  among  Angiosperms,  where  it  also  in- 
cludes strobili.  The  attempt  of  the  older  morphology  to  estab- 
lish a  definite  conception  for  a  flower,  and  to  force  all  of  the 
sporophyll-bearing  structures  of  Seed-plants  into  this  concep- 
tion w^as  exceedingly  unfortunate. 

The  development  of  floral  leaves  among  Angiosperms  seems 
to  be  connected  with  the  evolution  of  entomophily,  which  has 
resulted  in  immense  diversity  in  the  details  of  floral  structure, 
but  such  details  are  quite  foreign  to  the  purpose  of  this  book. 
The  origin  of  floral  leaves,  however,  is  a  question  that  must 
be  considered. 

That  all  floral  leaves  are  derived  from  sporophylls  may  be 
said  to  be  the  current  view,  as  stated  by  A.  P.  De  Candolle  in 
1817,  and  by  many  subsequent  writers,  notably  Celakovsky  in 
1896  and  1900.  Goebel,  however,  in  his  recent  Organogra- 
phie  der  Pflanzen,  claims  that  while  in  a  large  number  of  cases 
floral  leaves  may  be  derived  from  sporophylls,  as  in  Nymphaea, 
etc.,  they  are  often  derived  from  "  bracts."  For  example,  he 
calls  attention  to  certain  anemones  in  which  the  involucre  be- 
comes the  calyx  and  this  in  turn  may  become  petaloid.  In  other 
words,  he  claims  a  double  origin  for  floral  leaves,  namely,  spo- 
rophylls and  foliage  leaves,  and  whichever  their  origin  the 
result  is  the  same.  It  may  be  of  interest  to  note  that  GoebeFs 
definition  of  a  flower,  a  definition  originally  proposed  by 
Schleiden,  is  "  a  shoot  beset  with  sporophylls/7  which  of  course 


10  MORPHOLOGY  OF  ANGIOSPERMS 

includes  certain  Pteridophytes  among  flowering  plants.  It  is 
certainly  more  in  accord  with  present  morphological  concep- 
tions not  to  limit  too  rigidly  the  possible  origin  of  a  structure, 
and  from  this  point  of  view  it  seems  reasonable  that  floral  leaves 
in  general  may  have  been  derived  from  contiguous  structures 
both  above  and  below. 

It  is  not  always  easy  to  delimit  a  flower  exactly  from  the 
vegetative  shoot,  for  there  are  numerous  illustrations  of  grada- 
tions between  foliage  and  floral  leaves ;  but  for  all  ordinary 
purposes  four  different  organs  are  readily  recognized  as  enter- 
ing into  the  structure  of  a  highly  developed  flower.  The  dis- 
carded doctrine  of  metamorphosis  assumed  that  such  a  flower 
is  the  type,  from  which  all  others  are  the  modified  descendants, 
and  this  conception  is  perpetuated  in  terminology.  The  same 
conception  dominates  also  in  nearly'  all  presentations  of  floral 
diversities,  as  it  is  well-nigh  impossible  to  abandon  at  once  all 
the  terms  of  an  obsolete  conception  and  remain  intelligible. 
It  has  been  a  very  prevalent  conception,  therefore,  that  flowers 
of  simpler  structure  than  the  assumed  type  are  reduced  forms. 
There  are  certain  cases  in  which  this  seems  clear,  as  in  the 
relation  of  Lemna  to  the  Araceae;  but  the  vast  majority  of 
simpler  flowers  are  better  regarded  as  primitive  than  as  re- 
duced forms.  At  present  this  is  at  least  a  valuable  working 
hypothesis,  for  it  coincides  in  general  with  the  morphological 
and  historical  evidence  concerning  relationships,  as  well  as 
with  the  doctrine  of  evolution. 

—  Accepting  the  evidence  that  the  simpler  flowers  are  for  the 
most  part  the  more  primitive  forms  rather  than  reduced  ones, 
certain  prominent  tendencies  in  the  evolution  of  the  flower, 
admirably  presented  by  Engler,  may  be  discussed.  It  must  be 
understood,  however,  that  only  general  tendencies  are  traced, 
for  the  actual  lines  of  descent  can  not  be  determined  by  our 
present  knowledge. 

The  naked  flower  with  one  or  more  free  sporophylls  may 
be  regarded  as  the  most  primitive  form.  In  fact,  it  is  an 
angiospermous  flower  without  the  characteristic  floral  leaves. 
Such  a  flower  may  sometimes  represent  a  case  of  reduction, 
but  its  persistent  association  with  plants  recognized  as  primi- 
tive from  other  testimony  is  very  strong  evidence  that  it  is  a 
primitive  condition  of  the  flower.  From  this  stage  a  series 


THE  FLOWER  11 

can  be  arranged  illustrating  the  gradual  development  and  dif- 
ferentiation of  the  two  floral  envelopes.  Foliar  members, 
whether  derived  from  foliage  leaves  or  sporophylls,  become 
more  and  more  definitely  associated  with  the  sporophylls,  until 
they  may  be  regarded  as  constituting  an  inconspicuous,  bract- 
like  perianth.  They  gradually  appear  in  two  definite  sets  and 
become  more  conspicuous,  and  sooner  or  later  show  the  petaloid 
texture  and  coloration.  The  final  stage  is  a  completely  differ- 
entiated calyx  and  corolla,  with  their  characteristic  differences. 
This  tendency  to  produce  a  completely  differentiated  calyx  and 
corolla  has  resulted  in  its  attainment  by  most  flowers,  but  there 
are  numerous  cases  in  which  even  near  relatives  have  not  made 
the  same  progress  in  this  regard.  For  example,  the  phenom- 
enon styled  apetaly  may  be  observed  in  flowers  whose  nearest 
relatives  have  a  distinct  calyx  and  corolla.  While  some  cases 
of  apetaly  may  be  explained  as  the  suppression  of  a  set  of  floral 
envelopes,  there  are  certainly  cases  in  which  it  means  that  the 
two  sets  have  never  become  differentiated.  This  indicates  that 
progress  made  in  a  single  direction  can  not  be  used  as  a  cri- 
terion of  relationship.  In  general,  however,  it  must  remain 
true  that  a  flower  with  completely  differentiated  calyx  and 
corolla,  other  things  being  equal,  is  of  higher  rank  than  a 
flower  which  has  not  attained  this  differentiation. 

Among  the  most  primitive  flowers  the  floral  axis  tends  to 
elongate,  and  the  members  appear  in  indefinite  numbers  along 
a  low  spiral.  In  more  highly  developed  flowers  the  growth  of 
the  axis  in  length  is  checked  at  a  very  early  period,  so  that  the 
spiral  along  which  the  members  successively  appear  becomes 
lower  and  lower,  until  it  has  only  a  theoretical  existence,  pass- 
ing into  successive  cycles,  which  eventually  become  limited  in 
number.  With  the  appearance  of  definite  cycles  the  number  of 
members  appearing  in  each  one  becomes  limited,  the  limit  in 
Monocotyledons  being  prevailingly  three,  and  in  Dicotyledons 
five  or  four.  It  is  to  be  noted  that  the  cyclic  arrangement  is 
not  attained  simultaneously  by  all  the  sets  of  a  single  flower. 
For  example,  in  many  species  of  Ranunculus  the  sepals  and 
petals  are  cyclic,  or  approximately  so,  while  the  stamens  and 
carpels  are  distinctly  spiral.  This  tendency  is  so  well-marked 
and  so  uniformly  displayed  that  Engler  has  used  it  as  a  basis 
for  dividing  Monocotyledons  into  two  great  series,  the  "  spiral 


12  MORPHOLOGY  OF  ANGIOSPERMS 

series  "  comprising  all  those  families  that  show  the  spiral  tend- 
ency in  any  of  the  floral  sets,  and  the  "  cyclic  series  "  compris- 
ing all  those  whose  flowers  are  completely  cyclic,  the  former 
series  including  all  the  more  primitive  families.  There  is  no 
reason  why  this  same  distinction  can  not  be  applied  also  in  a 
general  way  to  the  Archichlamydeae.  This  gradual  transition 
of  flowers  from  the  spiral  to  the  cyclic  condition  is  one  of  the 
best-marked  tendencies  in  their  evolution,  and  has  the  advan- 
tage of  being  represented  by  innumerable  intermediate  stages. 
All  of  those  families  which  are  recognized  as  being  of  the  high- 
est rank  have  completely  cyclic  flowers,  with  members  appearing 
in  definite  and  low  numbers,  notably  illustrated  by  the  whole 
group  Sympetalae. 

There  is  a  marked  tendency  in  flowers  for  the  members 
of  a  single  set  to  lose  their  identity  and  to  develop  en  masse, 
a  phenomenon  called  "  coalescence  "  by  the  older  morphologists, 
under  the  impression  that  separate  members  had  united.  This 
congenital  union  is  to  be  distinguished  from  such  a  mechanical 
union  as  is  shown  by  the  anthers  of  Compositae.  In  the  organ- 
ogeny  of  such  a  flower  it  is  to  be  observed  that  in  the  meriste- 
matic  zone  from  which  a  certain  set  is  to  develop,  the  different 
members  first  appear  as  separate  primordia,  but  sooner  or  later 
the  whole  zone  shares  in  the  growth  and,  the  axial  growing 
point  being  checked,  an  annular  structure  arises  that  gradually 
assumes  the  size  and  form  of  the  mature  organ  (Fig.  1).  It 
has  been  claimed  that  this  is  a  toral  uprising  and  that,  for 
example,  the  tubular  portion  of  a  sympetalous  corolla  is  mor- 
phologically torus,  but  there  seems  no  more  reason  for  this 
supposition  than  to  regard  an  individual  petal  as  a  toral  up- 
rising. It  is  merely  the  difference  between  development  from 
the  meristematic  zone  at  certain  points  and  at  all  points.  As 
is  well  known,  this  development  of  the  whole  zone  may  begin 
almost  at  once,  or  may  be  deferred  until  the  set  is  nearly  mature, 
resulting  in  every  stage  of  separation  in  the  members,  from  a 
completely  tubular  structure  to  one  that  is  tubular  only  at  base. 
Or  the  zone  may  develop  for  a  time  in  two  sections  and  later 
en  masse,  resulting  in  the  so-called  bilabiate  structure.  Further 
inequalities  in  the  time  and  rate  of  development  result  in 
various-  irregularities.  In  any  event,  this  tendency  to  zonal 
development  rather  than  the  maintenance  of  separate  points  of 


THE  FLOWER  13 

development  is  persistent  among  flowers,  the  first  set  showing 
it  being  the  carpels,  resulting  in  syncarpy.  The  zonal  develop- 
ment of  the  corolla,  however,  or  sympetaly,  accords  with  so 
many  other  characters  indicating  natural  relationships  that  it 
has  been  used  to  designate  and  even  to  define  the  great. 'group 
Synipetalae.  This  is  probably  pressing  a  single  character  too 
far,  for  there  is  evidence  that  the  result  has  been  to  do  violence 
to  certain  natural  relationships,  and  to  make  certain  unnatural 
groupings.  This  tendency  to  zonal  development  is  found  in 
every  floral  set,  and  those  flowers  that  show  it  are  certainly 
to  be  regarded  as  of  higher  rank  than  those  that  do  not. 

Among  the  more  primitive  flowers  each  cycle  arises  sep- 
arately from  the  growing  point,  its  members  remaining  separate 
or  the  whole  meristematic  zone  entering  more  or  less  completely 
into  the  outgrowth.  The  insertion  of  each  cycle  is  definitely 
below  that  of  the  next  inner  cycle,  resulting  in  an  hypogynous 
flower  (Fig.  1,  A).  That  hypogyny  is  a  primitive  condition  of 
the  flower  is  a  statement  that  does  not  seem  to  need  discussion. 
The  tendency  to  zonal  development,  however,  is  carried  farther 
when  a  whole  region  arising  en  masse  produces  two  or  more 
•cycles  of  floral  members.  In  the  simplest  cases  two  cycles  are 
thus  produced,  as  is  illustrated  by  the  strong  tendency  of  the 
pe'taliferous  and  staminiferous  cycles  to  have  a  common  origin 
in  sympetalous  flowers,  resulting  in  the  appearance  of  "  stamens 
inserted  on  the  tube  of  the  corolla."  The  same  tendency  is 
shown  among  orchids,  in  which  the  whole  region  for  the  devel- 
opment of  stamens  and  carpels  arises  in  a  single  body,  forming 
the  characteristic  gynostemium  or  "  column."  While  these  may 
he  regarded  as  special  tendencies  of  certain  groups,  rather  than 
of  flowers  in  general,  there  are  other  instances  that  seem  to 
belong  to  the  general  evolution  of  the  flower.  In  certain  cases 
the  region  of  the  growing  point  belonging  to  the  carpels  ceases 
to  develop,  while  the  rest  of  the  growing  point  continues  to 
develop  en  masse,  forming  a  cup  or  urn-like  outgrowth,  from 
the  rim  of  which  the  three  outer  sets  develop  separately,  form- 
ing the  pe rig y nous  flower  (Fig.  1,  B).  In  this  case  the  carpels 
arise  from  what  seems  to  be  a  depression  in  the  center  of  the 
torus,  but  which,  of  course,  is  the  region  of  checked  growth. 
Perigyny  is  chiefly  displayed  among  families  of  the  Archi- 
chlamydeae. 


MORPHOLOGY  OF  ANGIOSPERMS 


Far  more  general  is  the  tendency  to  epigyny,  in  which  the 
checking  of  apical  growth  and  the  continued  growth  of  the  rest 
of  the  growing  point  results  in  an  ovule-bearing  cavity  grad- 


B 


D 

Fio.  1.— "Diagram  to  illustrate  the  morphology  of  typical  flowers.  A,  hypogynous; 
-ff,  perigynous ;  <?,  epigynous ;  Z>,  epigynous  with  prolonged  '  calyx  tube.'  Recep- 
tacle is  dotted  ;  carpels  are  cross-lined ;  '  perianth  tube,'  or  '  calyx  tube,'  vertically 
lined ;  sepals,  petals,  and  stamens  are  unshaded,  but  may  be  distinguished  by  their 
relative  positions." — After  GANONG.* 

ually  roofed  over  by  the  carpels.     From  the  top  of  the  ovary 

thus  developed  the  four  sets  of  floral  members  develop  as  usual, 

those  of  each  set  remaining  independent,  or  a  cycle  developing 

*  GANONG,  W.  F.     The  Teaching  Botanist.     New  York.     1899. 


THE  FLOWER  ^  15 

en  masse,  or  two  cycles  (especially  petaliferous  and  staminifer- 
ous)  having  a  common  origin  (Fig.  1,  C,  D).  Goebel  holds  (Or- 
ganographie)  that  at  least  in  some  epigynous  flowers  (as  Pirns 
Mains)  the  carpels  do  not  merely  roof  the  ovular  cavity  but  also 
line  it,  basing  the  claim  upon  a  study  of  the  meristematic  tissue ; 
in  which  case  the  wall  of  the  so-called  "  ovary  "  is  toral  without 
and  carpellate  within.  It  is  to  be  expected  that  numerous  in- 
termediate stages  between  complete  hypogyny  and  extreme 
epigyny  will  be  displayed,  as  may  be  inferred  even  from  the 
doubtful  phrases  employed  by  taxonomists  to  describe  them. 
It  also  seems  to  be  a  safe  conclusion,  since  epigyny  is  con- 
stantly associated  with  the  most  specialized  groups  of  each  great 
division,  as  Orchidaceae  among  Monocotyledons,  Umbelliferae 
among  Archichlamydeae,  and  Compositae  among  Sympetalae, 
that  it  is  a  mark  of  higher  rank  than  hypogyny  in  any  evolu- 
tionary series. 

The  tendency  for  the  members  of  a  floral  set  to  develop 
unequally,  resulting  in  zygomorphy  or  various  forms  of  "  irreg- 
ularity," is  not  general,  and  can  not  be  applied  so  broadly  as 
can  the  tendency  to  the  cyclic  arrangement  or  to  epigyny.  In 
certain  groups,  however,  it  is  very  pronounced  as  a  special 
character,  as  Orchidaceae  among  Monocotyledons,  Legumi- 
nosae  among  Archichlamydeae,  and  Personales  among  Sympet- 
alae.  The  occurrence  of  zygomorphy  in  relatively  primitive 
as  well  as  in  highly  specialized  groups  indicates  that  it  is  to  be 
regarded  as  a  special  rather  than  a  general  tendency;  and  yet, 
other  things  being  equal,  the  zygomorphic  flower  is  to  be  re- 
garded as  of  higher  rank  in  any  given  evolutionary  series  than 
the  actinomorphic  flower.  Diversities  resulting  from  inequali- 
ties of  growth  are  often  described  in  terms  of  symmetry,  a 
term  that  unfortunately  has  two  applications  in  connection 
with  the  flower,  for  its  well-known  biological  use  by  Sachs 
found  it  already  used  to  designate  a  flower  "  in  which  the  mem- 
bers of  all  the  cycles  are  of  the  same  number."  In  its  biological 
sense  a  symmetrical  flower  is  one  "  that  can  be  divided  into 
two  similar  halves,  or  the  parts  of  which  are  radially  disposed 
around  a  central  point."  The  terms  "  monosymmetrical "  and 
"  poly  symmetrical  "  are  logical,  but  not  better  than  the  older 
terms  of  Eichler,  "  zygomorphic  "  and  "  actinomorphic."  How- 
ever, the  phenomena  of  floral  symmetry  are  not  well  expressed 


16  MORPHOLOGY  OF  ANGIOSPERMS 

<  in  two  categories,  and  three  have  been  proposed,  as  follows:  (1) 
actinomorphicj  in  which  the  planes  of  symmetry  are  as  numer- 
ous as  the  members  of  a  cycle;  (2)  isobilateralj  in  which  there 
are  two  planes  of  symmetry,  but  the  halves  produced  by  one 
plane  are  unlike  those  produced  by  the  other  (Dicentra,  Cru- 
cifefae,  etc.)  ;  and  (3)  zygomorphic,  in  which  there  is  only  one 
plane  of  symmetry  (Fig.  2).  These  categories  are  expressions 
of  certain  laws  of  growth,  and  that  they  are  somewhat  funda- 


2. — A,  radial  symmetry  (Lilium  tigrinum);  i?,  isobilateral  symmetry  (Capsella 
Bursa-pastoris)  ;  f,  zygomorphic  symmetry  (Scrophularia  nodosa). 

mental  may  be  inferred  from  the  fact  that  they  are  persistent 
through  great  groups  of  plants. 

I^While  these  and  other  evolutionary  tendencies  are  to  be 
observed  among  flowers,  it  is  evident  that  they  are  not  neces- 
sarily expressed  simultaneously.  For  example,  the  spiral  and 
cyclic  arrangements  are  associated  in  Ranunculus,  zygomorphy 
is  associated  with  polypetaly  and  hypogyny  among  the  papil- 
ionaceous Leguminosae,  epigyny  is  associated  with  polypetaly 
among  the  Umbelliferae,  and  sympetaly  and  zygomorphy  are 
associated  writh  hypogyny  among  the  Labiatae.  It  is  among 
the  Compositae  that  practically  every  evolutionary  tendency 
mentioned  finds  its  highest  expression.  It  is  only  by  striking 
an  average  that  such  characters  may  be  used  in  roughly  placing 
a  family  in  its  evolutionary  position,  commonly  called  its 
"  relative  rank." 

A  The  classic  memoir  on  the  organogeny  of  the  flower  is 
Payer's  Traite  d'organogenie  de  la  fleur  (1857),  but  the  sub- 
ject has  not  been  developed  since  as  it  deserves.  In  the  case 
of  spiral  flowers,  in  which  the  torus  elongates  more  or  less,  the 


I  J 


FIG.  S.—  Cnicus  arvensis.  Floral  development:  A,  receptacle  almost  evenly  convex; 
appearance  of  papillae  to  become  flowers ;  <?,  a  single  papilla  more  advanced,  show- 
ing beginning  of  corolla ;  /),  corolla  more  prominent ;  E,  stamens  distinguishable ; 
F,  carpels  and  pappus  (calyx)  evident;  G,  carpels  beginning  to  form  cavity  of 
ovary ;  H.  ovule  readily  distinguishable ;  /,  ovule  showing  megaspore  mother-cell 
and  single  thick  integument :  5,  bract  of  involucre ;  c,  corolla ;  *,  stamen ;  0,  carpel ; 
p.  pappus  (calyx).  A-H  x  50  ;  I  x  100. 

17 


18  MORPHOLOGY  OF  ANGIOSPERMS 

members  appear  in  acropetal  succession  along  a  continuous  low 
spiral,  and  just  when  one  set  of  members  stops  and  the  next 
begins  is  indefinite  within  certain  usual  limits.  There  seems 
no  doubt  in  this  case  that  the  primordia  are  indifferent  up  to 
a  certain  stage  of  development,  and  that  the  particular  organ 
produced  depends  upon  something  outside  of  the  essential  con- 
stitution of  the  primordium  itself.  In  the  case  of  cyclic  flowers, 
in  which  toral  growth  in  length  has  been  checked  and  there  has 
been  growth  in  diameter,  the  acropetal  succession  of  members 
is  often  very  much  interfered  with.  The  "  disturbances  "  that 
arise  in  the  torus  by  substituting  growth  in  diameter  for  growth 
in  length  account  not  only  for  the  breaking  up  of  the  acropetal 
succession,  but  also  for  the  inequality  of  members  of  the  same 
cycle,  or  of  different  regions  of  the  cycle.  It  is  evident  that  in 
the  case  of  cyclic  flowers  organogeny  must  'deal  'not  only  with 
the  succession  of  cycles,  but  also  with  the  succession  of  mem- 
bers in  each  cycle.  Definite  data  in  reference  to  these  points 
are  not  so  available  as  they  should  be,  but  a  few  illustrations 
may  be  cited. 

For  the  majority  of  cyclic 'flowers  it  seems  to  be  assumed 
that  the  cycles  appear  in  acropetal  succession — namely,  sepals, 
petals,  stamens,  carpels — and  that  the  members  of  each  cycle  are 
practically  synchronous  in  origin,  but  it  is  probable  that  this 
assumption  is  gratuitous.  While  theoretically  it  may  be  as- 
sumed that  the  cycles  should  arise  in  acropetal  succession,  the 
fact  that  they  do  not  in  many  observed  cases  indicates  that 
they  may  not  in  many  more  cases ;  and  the  synchronous  ap- 
pearance of  the  members  of  a  single  cycle  is  unsound  as  a 
theoretical  assumption.  Hofmeister  *  records  that  in  Rosa, 
Potentilla,  and  Rubus  the  primordia  of  the  carpels  appear  be- 
fore those  of  the  stamens  have  reached  the  full  number,  and 
that  in  Hypericum  calycinum  the  primordia  of  the  sepals  ap- 
pear after  those  of  the  stamens.  It  is  also  generally  known 
that  among  the  Compositae  (Fig.  3),  D^psaceae,  Valerianaceae, 
and  Rubiaceae,  in  which  the  sepals  are  much  reduced  or  modi- 
fied, their  primordia  do  not  appear  until  after  those  of  the 
stamens  and  carpels;  and  that  among  the  Cruciferae  (in  Cap- 
sella,  at  least)  (Fig.  4)  the  petals  are  the  last  members  to 

*  HOFMEISTER,  W.    Allgemeine  Morphologic  der  Gewachse.    Leipzig.    1868. 
p.  462. 


THE  FLOWER 


appear.  Webb  *  has  recently  observed  in  Astilbe  that  the 
order  of  succession  of  floral  cycles  is  sepals,  inner  stamens,  car- 
pels, outer  stamens,  and  petals.  In  this  case  there  'is  an  acro- 


FIG.  4. — Capsella  Bursa-pastoris.    Floral  development:  A,  floral  axis  before  appearance 
of  floral  organs ;  B,  appearance  of  sepals ;  6T,  appearance  of  stamens ;  carpels  barely 
distinguishable ;  Z>,  appearance  of  petals :  s,  sepals ;  m,  stamens ;  c,  carpels ;  p,  petals 
i      x  130. 

petal  succession  of  certain  cycles,  followed  by  a  basipetal  succes- 
sion of  the  remaining  ones.  The  remarkable  case  of  the  flower 
of  the  Primulaceae,  noted  by  Pfeffer,f  is  also  familiar,  in 

*  WEBB,  J.  E.  A  Morphological  Study  of  the  Flower  and  Embryo  of  Spi- 
raea. Bot.  Gazette  33 :  451-460.  figs.  27.  1902.  For  correction  of  names,  see 
REHDER  in  Bot.  Gazette  34  :  246.  1902. 

f  PFEFFER,  W.  Zur  Bliithenentwicklung  der  Primulaceen  und  Ampelideen. 
Jahrb.  Wiss.  Bot.  8 :  194-215.  1872. 


20  MORPHOLOGY  OF  ANGIOSPERMS 

which  the  primordia  of  the  petals  appear  after  those  of  the 
stamens,  and  each  apparently  from  the  dorsal  surface  of  a  young 
stamen.  The  conclusion  that  the  so-called  petals  of  this  family 
are  not  morphologically  petals,  but  stamineal  outgrowths,  is 
unnecessary,  since  the  phenomenon  can  be  more  logically  in- 
terpreted as  a  case  in  which  the  primordia  of  stamen  and  petal 
have  a  common  origin,  entirely  analogous  to  the  sympetalous 
corolla  with  stamens  "  inserted  on  its  tube,"  but  in  which  the 
separate  primordia  of  the  petals  have  been  delayed  in  their 
appearance.  Such  examples  as  those  enumerated  above  simply 
serve  to  emphasize  the  desirability  of  a  more  serious  and  sys- 
tematic investigation  of  the  whole  subject. 

In  the  case  of  members  of  a  single  cycle,  it  is  a  question 
whether  their  primordia  ever  appear  simultaneously,  although 
they  may  appear  in  rapid  succession.  In  zygomorphic  flowers, 
however,  the  succession  is  probably  always  evident.  For  ex- 
ample, Goebel  *  cites  the  case  of  the  papilionaceous  Legumino- 
sae,  in  which  the  anterior  median  sepal  first  appears,  then  those 
to  the  right  and  left  of  it  simultaneously,  and  finally  the  two 
obliquely  posterior  ones ;  but  before  these  last  are  evident  the 
two  obliquely  anterior  petals  appear,  and  after  them  the  other 
three  in  the  same  order  as  the  corresponding  sepals.  This 
succession  proceeds  right  and  left  from  the  anterior  member 
to  the  posterior.  In  other  known  cases,  however,  as  in  Reseda, 
according  to  Payer,  the  succession  is  right  and  left  from  the 
posterior  member  to  the  anterior. 

It  must  also  be  noted  that  a  meristematic  zone  giving  rise 
to  a  set  of  members  may  add  to  the  set  later  or  even  duplicate 
it,  giving  rise  to  the  well-known  interposition  of  new  members 
or  new  sets.  For  example,  it  is  stated  that  among  the  Gera- 
niaceae,  Kutaceae,  and  Zygophyllaceae  a  new  cycle  of  five  sta- 
mens is  interposed  among  the  five  already  formed;  and  that 
in  Aceraceae  and  Sapindaceae  two  to  four  stamens  are  inter- 
calated in  the  complete  cycle  of  five  previously  formed.  This 
later  interposition  of  new  sets  or  new  members  has  been  re- 
corded chiefly  for  stamens,  and  is  a  prolific  source  of  inter- 
ference with  the  "  symmetry  "  of  numbers. 

All  seed-bearing  plants  are  necessarily  dioecious  since  they 

*  GOEBEL,  C.     Outlines  of  Classification  and  Special  Morphology.     English 
translation.     1887.     p.  424. 


THE  FLOWER  21 

are  heterosporous.  So  far  as  there  is  any  advantage  in  this 
habit,  however,  it  is  practically  lost  if  stamens  and  carpels  are 
present  in  the  same  flower  or  upon  the  same  plant.  Morpho- 
logically the  gametophytes  are  unisexual,  but  in  fact  they  are 
dependent  upon  the  same  individual.  Any  physiological  advan- 
tage, therefore,  that  comes  from  the  crossing  of  individuals 
must  be  secured  by  pollination  or  by  the  separation  of  stamens 
and  carpels  upon  different  individuals.  It  is  unfortunate  that 
the  term  "  dioecious  "  has  two  distinct  morphological  applica- 
tions, referring  to  the  sexual  differentiation  of  individuals 
among  the  lower  plants,  and  to  the  sporangial  differentiation 
of  individuals  among  seed-bearing  plants;  but  from  the  phys- 
iological standpoint  the  distinction  probably  does  not  exist.  As 
a  consequence,  the  dioecious  habit  in  effect  is  secured  in  certain 
seed-plants  by  the  development  of  monosporangiate  individuals, 
and  it  is  perhaps  significant  that  this  habit  not  only  prevails 
among  the  more  primitive  seed-bearing  plants,  but  is  associated 
in  the  main  with  wind-pollination.  Among  the  higher  Angio- 
sperms  the  effect  of  the  dioecious  habit  is  secured  for  bisporan- 
giate  plants  by  means  of  insect-pollination.  It  follows  from 
this  point  of  view  that  neither  the  monosporangiate  nor  the 
bisporangiate  habit  can  be  regarded  as  in  itself  the  more  primi- 
tive. The  former  habit  prevails  among  the  more  primitive 
families  because  they  are  necessarily  anemophilous ;  while  the. 
latter  prevails  among  the  higher  families  because  insect  polli- 
nation does  not  necessitate  the  monosporangiate  habit.  It 
should  be  noted  that  Goebel  (Organographie)  regards  the 
bisporangiate  condition  as  primitive,  the  monosporangiate 
being  derived  from  it  by  reduction.  This  can  be  demonstrated 
in  certain  cases,  but  the  monosporangiate  condition  is  probably 
the  primitive  one  in  many  of  the  more  primitive  angiospermous 
families.  In  any  event,  the  monosporangiate  and  bisporan- 
giate habits  are  not  always  settled  ones.  For  example,  in  the 
monosporangiate  Amarantus  retroflexus  there  are  occasional 
bisporangiate  flowers;  while  in  monosporangiate  and  dioecious 
willows  both  catkins  may  appear  on  the  same  individuals,  and 
the  catkins  themselves  may  be  mixed  (staminate,  pistillate,  and 
bisporangiate).  It  follows  also  that  there  may  be  monosporan- 
giate members  in  all  great  groups  (as  Ranunculaceae),  or  even 
in  bisporangiate  genera  (as  Rumex  and  Lychnis),  for  this  habit 


22  MORPHOLOGY  OF  ANGIOSPERMS 

is  probably  not  a  hindrance  to  any  form  of  pollination,  and  cer- 
tainly prevents  self-pollination.  Cross-pollination  by  wind  or  by 
insects,  therefore,  appears  as  an  offset  to  the  loss  of  any  advantage 
originally  gained  by  the  dioecious  habit ;  and  the  appearance  of 
monosporangiate  individuals  in  any  Angiosperm  group  does  not 
imply  a  tendency  toward  a  more  primitive  or  more  advanced 
condition.  For  example,  the  monosporangiate  habit  of  poplars  is 
no  more  indicative  of  -a  primitive  condition  than  is  the  monospo- 
rangiate habit  of  certain  Compositae  of  an  advanced  condition. 
The  older  morphologists  considered  the  floral  members  as 
morphologically  leaves,  and  presented  proofs  which  to  them 
seemed  decisive,  such  as  the  leaf-like  position  and  intergrading 
of  members,  and  various  malformations,  among  which  are  the 
so-called  "  reversions.'7  This  conclusion  was  controlled  by  the 
prevailing  doctrine  of  metamorphosis,  and  under  its  guidance 
nothing  seemed  clearer  than  that  stamens  and  carpels  are  trans- 
formed leaves.  .  While  sepals  and  petals  may  be  regarded  as 
often  leaves  more  or  less  modified  to  serve  as  floral  envelopes, 
and  are  not  so  different  from  leaves  in  structure  and  function 
as  to  deserve  a  separate  morphological  category,  the  same  claim 
can  not  be  made  for  stamens  and  carpels.  They  are  very  an- 
cient structures,  of  uncertain  origin,  for  it  is  quite  as  likely 
that  leaves  are  transformed  sporophylls  as  that  sporophylls  are 
transformed  leaves.  It  is  a  rigid  morphology,  however,  domi- 
nated by  the  doctrine  of  - "  types,"  that  denies  to  an  organ  so 
thoroughly  established  as  the  stamen  of  Angiosperms  a  mor- 
phological individuality.  One  might  almost  as  well  deny  to 
the  leaf  itself  a  morphological  individuality  because  it  did  riot 
always  exist  as  a  distinct  organ.  Just  how  long  an  organ  must 
maintain  its  independence  before  it  can  be  recognized  as  a 
morphological  unit  is  not  easy  to  say,  but  stamens  and  carpels 
seem  to  have  earned  the  right.  To  call  a  stamen  a  modified 
leaf  is  no  more  sound  morphology  than  to  call  a  sporangium 
derived  from  a  single  superficial  cell  a  modified  trichome.  The 
cases  of  "  reversion  "  cited  are  easily  regarded  as  cases  of  re- 
placement. Lateral  members  frequently  replace  one  another, 
but  this  does  not  mean  that  one  is  a  transformation  of  the  other. 
For  example,  in  1889  Barber  *  observed  a  Nympliaea  in  which 

*  BARBER,  C.  A.     On  a  Change  of  Flowers  to  Tubers  in  Nymphaea  Lotus, 
var.  monstrosa.     Annals  of  Botany  4 :  105-116.  pi.  5.  1889. 


THE  FLOWER  23 

foliage  leaves  had  replaced  all  the  floral  members  within  the 
calvx  and  the  end  of  the  axis  had  become  much  swollen.  It  is 
probable  that  the  latter  fact  was  responsible  for  the  former,  and 
that  a  growing  axis  put  forth  leaves,  as  it  usually  does ;  but  the 
inference  that  these  leaves  represent  the  replaced  floral  mem- 
bers in  any  morphological  sense  has  no  logical  connection  with 
the  facts  observed.  Such  cases  as  that  of  the  ordinary  flowers 
of  Nymphaea,  in  which  stamens  seem  to  be  gradually  differ- 
entiated from  petals,  present  no  difficulty  wThen  one  notes  the 
remarkable  indifference  of  sporangia  to  the  nature  of  the  mem- 
ber upon  which  they  appear.  Because  microsporangia  appear 
occasionally  upon  an  axial  structure  it  might  as  well  be  argued 
that  stamens  are  transformed  stems.  The  stamens  and  carpels 
are  just  as  definite  morphological  structures  as  are  foliage 
leaves,  with  just  as  distinct  functions,  and  should  be  so  re- 
garded, whatever  may  have  been  their  historical  origin.  Stamen  % 
and  leaf  probably  merge  into  one  another  in  history,  and  so  ] 
do  stem  and  leaf,  but  all  have  become  established  as  distinct  Jf 
organs. 

Further  details  as  to  the  varying  form  and  structure  of 
sepals  and  petals  are  of  no  special  morphological  significance, 
and  are  of  interest  chiefly  to  the  taxonomist  and  the  ecologist. 
The  stamens  and  carpels,  however,  are  so  intimately  associated 
with  essential  morphological  structures  that  some  further  de- 
tails in  reference  to  them  are  necessary. 

The  stamen  set  has  been  called  collectively  the  "  androe- 
cium,"  a  name  so  objectionable  to  the  morphologist  on  account 
of  its  sexual  significance  that  it  should  be  abandoned.  The 
stamen  is  an  organ  devoted  to  the  production  of  microsporangia, 
and  its  endless  diversity  of  form  and  position  is  related  more 
or  less  directly  to  the  needs  of  pollination.  The  term  "  anther  " 
is  one  of  convenience,  but  represents  a  morphological  complex 
made  up  of  sporangia  and  more  or  less  sporophyll  tissue.  The 
cooperation  of  sporophyll  and  sporangia  in  the  dehiscence  of 
the  latter  will  be  included  in  the  discussion  of  the  microsporan- 
gium,  as  well  as  those  various  differences  among  anthers  that 
have  to  do  with  the  number  and  behavior  of  their  sporangia. 
It  is  important  to  note  that  stamens  have  the  power  of  branch- 
ing, and  can  thus  multiply  sporangia.  Well-known  cases  are 
CaUothamnus,  in  which  the  branching  is  like  that  of  a  pinnate 
3 


24  MORPHOLOGY  OF  ANGIOSPERMS 

leaf ;  Ricinus,  in  which  repeated  forking  results  in  a  stamen, 
bearing  very  numerous  sporangia;  and  Hypericum,  in  which 
the  primordium  branches,  that  is,  produces  secondary  primor- 
dia,  the  common  base  of  the  tufted  cluster  not  being  recognized 
in  the  mature  condition.  The  case  of  zonal  development,  that 
is,  an  uprising  from  the  whole  staminiferous  zone,  and  also  the 
case  of  stamen  and  petal  or  stamen  and  carpel  regions  rising 
en  masse,  have  already  been  noted  in  connection  with  the  gen- 
eral tendencies  of  the  flower.  The  tendency  of  stamens  and 
of  carpels  to  become  more  or  less  coalescent  through  pressure  is 
also  well  marked,  as  in  the  anthers  of  Compositae  and  Lobe- 
liaceae,  and  in  some  cases  that  have  been  called  syncarpy.  It 
remains  to  note  the  fact  that  stamens  occur  in  all  stages  of 
abortion,  especially  to  be  observed  among  the  Personales,  from 
the  absence  of  sporangia  to  that  amount  of  abortion  that  is 
only  short  of  suppression.  Stamens  that  have  lost  their  normal 
function  are  generally  called  "  staminodia,"  but  they  may  as- 
sume various  forms  and  serve  a  variety  of  purposes.  In  certain 
cases,  as  notably  among  the  Labiatae,  the  claim  that  one  or 
more  stamens  have  been  suppressed  is  justified  by  their  pres- 
ence in  near  relatives,  combined  with  the  occurrence  of  unoc- 
cupied points  where  stamens  ordinarily  appear. 

The  carpel  set  has  been  called  collectively  the  "  gynoecium,"' 
a  term  that  also  should  be  dropped  from  morphological  ter- 
minology on  account  of  its  implication  of  sexuality.  The  carpel 
is  the  organ  most  intimately  related  to  the  megasporangia,  in- 
vesting them  more  or  less  completely,  but  not  always  producing 
them,  and  giving  name  to  the  Angiosperms.  Its  history  is  un- 
known, for  although  it  is  easy  to  imagine  it  derived  from  such 
open  carpels  as  are  found  among  Gymnosperms,  no  clear  inter- 
mediate stages  have  been  found.  At  all  events,  it  is  a  thor- 
oughly established  and  characteristic  organ.  The  term  ".ovary  " 
for  the  sporangium-bearing  cavity  is  particularly  unfortunate 
on  account  of  its  very  different  application  among  animals. 
To  avoid  this  confusion  Barnes  *  has  proposed  the  term  "  ovu- 
lary,"  but  even  this  contains  in  its  stem  the  sexual  implica- 
tion. The  style  is  definitely  related,  in  its  varying  form  and 
length,  to  the  problem  of  pollination,  and  upon  it  the  stig- 

*  BARNES,  C.  R.     Plant  Life.     1898.     p.  240. 


THE  FLOWER  25 

niatic  surface  is  developed  in  various  ways.  This  surface  is 
increased  in  area  by  the  enlargement  of  the  apex  of  the  style, 
by  its  branching,  or  by  being  developed  laterally  upon  the  style. 

One  of  the  essential  features  of  the  structure  of  the  carpel 
is  the  provision  for  the  progress  of  the  pollen-tube  from  the 
receptive  surface  to  the  sporangium  or  even  to  its  micropyle. 
A  specialized  and  continuous  nutritive  tissue  connects  these 
two  extremes,  often  confused  in  the  sporangial  chamber  with 
the  u  placenta,"  in  the  style  called  "  conducting  tissue,"  and 
upon  its  surface  the  "  stigma,"  but  forming  one  continuous 
tissue  system,  well  named  the  conducting  tissue.  It  is  unfor- 
tunate that  the  terminology  of  taxonomy  has  somewhat  di- 
verted attention  from  the  continuity  of  this  tissue,  for  in  it 
the  "  stigma  "  is  an  organ  distinct  from  the  style,  rather  than 
a  display  upon  the  surface,  often  modified  to  receive  it,  of  a 
special  tissue  of  the  style.  While  the  placenta  is  the  point  or 
line  of  sporangium  origin,  and  may  be  said  to  consist  of  spo- 
rangiogenic  tissue,  it  is  probably  true  that  much  of  the  out- 
growth that  stands  for  the  placenta  to  many  is  conducting 
tissue.  In  the  case  of  hollow  styles,  as  in  Lilium,  Butomus, 
Agave,  Erythronium,  Viola,  Campanula,  Barcodes,  etc.,  the 
conducting  tissue  lines  the  canal  as  a  glandular  layer,  or  in  some 
cases,  as  in  AnagalUs,  fills  up  a  hollow  style;  but  in  most  cases 
the  style  is  solid,  with  the  conducting  tissue  as  an  axial  strand. 
In  case  a  single  style  is  connected  with  two  or  more  sporangial 
chambers,  the  strand  of  conducting  tissue  branches  into  each 
chamber.  This  suggests  the  possibility  that  the  stylar  canal, 
with  its  lining  of  conducting  tissue,  may  represent  a  primitive 
angiospermous  condition,  and  that  the  larger  development  of 
this  tissue  has  resulted  in  the  prevailing  solid  style,  a  view  that 
is  also  suggested  by  the  development  of  the  style.  Of  course 
the  reverse  may  be  true,  and  the  stylar  canal  a  result  of  the 
breaking  down  or  rupture  of  the  axial  strand  of  conducting 
tissue. 

The  strong  tendency  to  a  congenital  development  of  carpels 
has  been  previously  noted,  and  this  justifies  the  use  of  the  term 
*'  pistil "  as  one  of  convenience,  although  it  does  not  stand  for  a 
morphological  unit.  It  is  applied  to  any  organization  of  car- 
pels that  appears  as  a  single  organ  with  one  ovary,  whether  one 
or  more  carpels  are  involved.  It  is  to  be  noted  that  the  term 


26  MORPHOLOGY  OF  ANGIOSPERMS 

"  ovary  "  also,  as  usually  applied,  has  no  definite  morphological 
significance,  referring  to  a  morphologically  single  sporangial 
chamber  or  to  a  combination  of  several  such  units,  and  these 
chambers  may  be  of  axial  as  well  as  of  carpellary  origin.  The 
various  ways  in  which  the  congenital  carpels  are  related  to  one 
another  in  a,  compound  pistil  are  of  great  service  in  taxonomy, 
afe  the  particular  structure  of  such  a  pistil  is  usually  charac- 
teristic of  great  families,  or  even  of  groups  of  higher  rank. 
These  details  of  structure  are  too  fully  presented  in  various 
texts,  however,  to  justify  their  repetition  here.  The  relation 
of  sporangia  to  carpels  is  an  important  subject  to  the  morpholo- 
gist,  and  will  be  considered  in  connection  with  the  development 
of  the  sporangia. 


CHAPTEK    III 


THE   MICBOSPOBANGIUM 

THE  microsporangia  of  Angiosperms  are  embedded  struc- 
tures, and  are  derived  from  the  outermost  layer  of  the  peri- 
blem.  Thus  far,  the  only  recorded 
exceptions  to  this  origin  are  Naias 
ftexilis,  and  probably  Zannichellia  15 
and  Lilaea  subulata,18  whose  micro- 
sporangia  are  claimed  by  Campbell 
to  be  derived  from  the  plerome  (Fig. 
5).  The  periblem  origin  of  the  spo- 
rangia seems  to  account  for  the  fact 
that  the  archesporium  is  superficial 
in  Pteridophytes  and  hypodermal  in 
Spermatophytes.  It  also  accounts  for 
the  indifference  of  the  sporangia  to 
the  morphological  nature  of  the  or- 
gan upon  which  they  appear.  In 
general,  they  occur  upon  a  lateral 
member  that  holds  the  same  relation 
to  the  axis  as  do  the  leaves,  and  in 
this  sense  it  may  be  called  a  leaf-like 
member.  Such  sporangia,  therefore, 
may  be  called  foliar,  and  the  struc- 
ture that  bears  them  a  sporophyll. 
In  certain  cases,  however,  the  sporan- 
gia are  derived  from  the  periblem 
of  the  axis,  and  such  may  be  called 
cauline.  In  each  case  the  resulting 
organ  is  a  stamen,  whether  in  the  po- 
sition of  a  leaf  or  \>f  an  axis.  The  freedom  with  which  micro- 
sporangia  are  sometimes  produced  may  be  illustrated  by  the 

27 


B 

FIG.  5. — Naias  flfxilis.  A,  young 
stamen  showing  "  integument " 
and  plerome  origin  of  arche- 
sporium ;  sporogenous  cells  rep- 
resented with  nuclei:  x  200. 
B,  later  stage;  x  TO.— After 

CAMPBELL.15 


28 


MORPHOLOGY  OF  ANGIOSPERMS 


willows,  notably  Salix  petiolaris,  in  which  Chamberlain  16  found 
microsporangia  in  the  "  placenta  "  of  the  ovary,  the  carpel  some- 
times being  wide  open  and  bearing  both  microsporangia  and 


FIG.  Q.—tSalix  petiolaris.  A,  microsporangia  in  wall  of  ovary ;  both  anatropous  and 
orthotropous  ovules.  B,  microsporangia  with  long  stalks  within  the  ovary  ;  pollen 
normally  developed ;  ovule  orthotropous.  C,  branching  stamen,  each  anther  with 
four  microsporangia;  anther  on  right  terminated  by  a  stigma;  x  50. — After  CHAM- 
BERLAIN.™ 

megasporangia,  and  in  some  cases  stigmas  developing  on  sta- 
mens (Fig.  6). 

The  cauline  origin  of  microsporangia  seems  to  have  been 
recorded  first  in  1868  in  the  case  of  Casuarina,  by  Kauff- 
mann ;  6  and  then  in  1869  for  the  species  of  Naias,  by  Magnus,7 
confirmed  in  1897  by  Campbell.15  In  1873  Warming8  made 
a  similar  record  for  Cyclanthera,  and  was  confirmed  by  Eng- 
ler  9  in  1876.  Rohrbach  5  discovered  cauline  microsporangia 
in  Typha-j  Goebel11  (p.  353)  states  that  they  occur  in  the 
"  unbranched  stamens  " ;  and  their  occurrence  in  T.  latifolia 
was  confirmed  by  Schaffner17  in  1897.  In  1897  Campbell15 
added  to  the  list  Z 'annichellia,  and  in  1898  Lilaea.18  In  1900 
Lotsy30  suggested  that  the  curious  stamen  of  Rhopalocnemis 
phalloides  (Balanophoraceae)  is  an  axial  structure. 


THE  MICROSPORANGIUM 


29 


It  is  reasonably  assured,  therefore,  that  cauline  micro- 
sporangia  occu^1  in  at  least  seven  genera,  both  Monocotyledons 
and  Dicotyledons  being  represented.  Upon  the  whole,  they 
seem  more  characteristic  of  the  primitive  members  of  these 
two  groups  than  of  the  more  highly  specialized  members,  but 
this  impression  may  disappear  with  further  investigation.  If 
the  cauline  origin  of  megasporangia  be  considered,  the  primi- 
tive character  of  this  feature  becomes  increasingly  uncertain, 
for  cauline  megasporangia  are  common  even  in  the  highest 
groups.  It  seems  probable,  therefore,  that  the  cauline  or  foliar 
origin  of  sporangia  among  Angiosperms  is  not  to  be  taken  as 
an  argument  for  or  against  the  primitive  character  of  the  group 
in  which  they  occur.  The  particular  organ  developing  micro- 
sporangia  was  probably  determined  not  by  its  morphological 
nature,  but  by  what  may  be  called  its  physiological  relations 
(Fig.  6).  Even  among  Pteridophytes,  the  sporangia  of  Lycopo- 
dium  are  foliar,  and  those  of  the  nearly  allied  Selaginella  cau- 
line; and  among  Gymnosperms  sporangia  have  both  origins. 
It  is  evident,  therefore,  that  the  distinguishing  morphological 


FIG.  7. — Lilium  philadelphicum.  Transverse  section  of  almost  mature  anther ;  nearly 
all  the  walls  separating  the  microsporangia  have  broken  down ;  highly  developed 
stomium  (*)  and  endothecium  (with  its  rib-like  thickenings)  very  prominent;  x  25. 
—From  a  drawing  by  W.  J.  G.  LAND. 

structure  is  the  sporangium  rather  than  any  member  of  the 
plant  body  from  which  it  may  arise. 

In  most  cases  the  stamen  produces  four  microsporangia 
(Fig.  7),  and  the  exceptions  noted  thus  far  are  by  n'o  means 


30  MORPHOLOGY  OF  ANGIOSPERMS 

numerous.  Caldwell  23  has  called  attention  to  the  occurrence 
of  what  might  be  regarded  a  single  microsporangium  in  Lemna  \ 
it  is  well  known  that  the  stamens  of  Asclepiadaceae  produce 
only  two  microsporangia ;  and  in  Hamamelis  (Shoemaker35) 
there  is  a  single  sporangium  to  each  "  pollen-sac."  Eight  mi- 
crosporangia had  long  been  observed  among  the  Mimoseae  when 
Engler  9  reported  a  still  larger  number.  Among  the  Orchida- 
ceae  Guignard  10  reports  eight  rnicrosporangia  in  the  stamen 
of  Calanthe  veratrifolia;  and  among  the  Onagraceae,  as 
in  Gaura,  more  than  four  microsporangia  are  suggested  by 
the  pollen-sacs  (see  Goebel,11  p.  369,  foot-note  2).  Among 
Loranthaceae  Van  Tieghem  13  says  that  the  number  of  pollen- 
sacs  is  exceedingly  variable,  ranging  from  one  to  an  indefinite 
number;  and  the  same  is  true  of  the  Balanophoraceae,  as  re- 
ported by  several  investigators.  Attention  should  be  called  to 
the  fact,  however,  that  the  number  of  sporogenous  masses  finally 
developed  may  not  necessarily  determine  the  number  of  spo- 
rangia, for  plates  of  sterile  tissue,  derived  from  sporogenous 
tissue,  have  been  observed  to  divide  a  single  mass  of  sporoge- 
nous tissue  into  two  or  more.  This  has  been  made  out  clearly 
by  Caldwell  23  in  the  case  of  Lemna  (Fig.  14)  ;  and  in  those 
cases  in  which  more  than  four  microsporangia  are  reported  a 
detailed  study  of  their  origin  is  desirable.  In  the  case  of 
branching  stamens,  referred  to  on  p.  23,  the  microsporangia 
may  become  very  numerous. 

The  time  for  the  formation  of  microsporangia  in  relation 
to  what  is  usually  called  "  the  growing  season "  has  not  re- 
ceived the  attention  it  deserves.  In  1896  Arma  Smith  14  re- 
ported that  she  had  discovered  the  pollen  mother-cells  of  Tril- 
lium dividing  in  the  spring  beneath  frozen  soil.  In  1897 
Chamberlain  16  called  attention  to  the  fact  that  the  microsporan- 
gia of  Salix  glaucophylla  are  in  the  mother-cell  stage  in  Oc- 
tober, and  that  they  pass  the  winter  in  this  condition.  In  1898 
the  same  investigator 20  reported  that  this  is  true  of  other 
species  of  Salix ;  that  in  Corylus  americana  (Fig.  8,  B)  and 
Alnus  glutinosa  the  midwinter  catkins  contain  pollen  ready  for 
shedding  with  the  generative  cell  formed;  that  in  Populus 
monilifera  (Fig.  8,  A)  the  primary  sporogenous  cells  are 
found  in  July  and  the  mother-cell  stage  in  October,  the  latter 
condition  persisting  through  the  winter;  and  that  in  Hepatica 


THE  MICROSPORANGIUM 


31 


the  mother-cell  stage  was  found  in  September,  and  fully  formed 
pollen  in  the  spring  while  the  ground  was  still  frozen.  Dug- 
gar  27  has  also  observed  that  the  microsporangia  of  Symplo- 
carpus  pass  the  winter  in  the  mother-cell  stage.  The  pollen 
mother-cells  of  Podopliyllum  peltatum  are  forming  the  tetrads 
when  the  young  plant  has  reached  the  surface  of  the  ground, 
so  that  in  all  probability  the  winter  is  passed  in  the  mother-cell 
stage.  Although  Conrad  29  found  stamens  well  formed  in  the 
winter  buds  of  Quercus  velutina, 
the  tissue  of  the  anther  was  still 
homogeneous.  These  records  mere- 
ly serve  as  an  indication  of  what 
may  be  expected  when  the  subject 
is  really  investigated.  It  is  evident 
that  the,  time  elapsing  between  the 
differentiation  of  the  archesporium 
and  pollination  is  often  much  longer 
than  has  been  ordinarily  supposed. 
It  would  seem  probable  that  in  gen- 
eral those  plants  whose  flowers  open 
early  in  the  season,  as  most  trees 
and  the  vernal  herbs,  develop  their 
microsporangia  before  the  end  of 
the  "  growing  season,"  and  that  the 
mother-cell  stage  is  the  usual  win- 
ter condition.  In  the  case  of  such 
plants,  therefore, 'the  earliest  stages 
in  the  history  of  the  microsporangia 
must  be  looked  for  during  the  latter 
half  of  the  growing  season  that  pre- 
cedes the  season  of  "  blooming." 
This  suggests  that  the  natural  end  of  a  growing  season  for  the 
sporophyte  is  the  attainment  of  the  mother-cell  stage  by  its  spo- 
rangia, which  is  really  the  limit  of  the  sporophyte  in  the  alterna- 
tion of  generations ;  and  the  natural  beginning  of  the  next  season 
is  the  reduction  division  and  the  beginning  of  the  gametophyte. 
Of  course  such  a  distinction  disappears  in  many  plants  whose 
seasonal  habits  are  different  from  those  we  have  been  consider- 
ing, but  it  suggests  a  natural  division  of  growth  betw«wfteasons, 
and  even  in  annuals  the  mother-cell  stage  is  a  prolonged  one. 


FIG.  8.  —  A,  Populus  monilifera, 
probably  spore  mother-cell  stage, 
Jan.  25, 1895 ;  x  600.  B,  Corylus 
americana,  pollen  ready  for  shed- 
ding, Dec.  7, 1897 ;  *  400.— After 

CHAMBERLAIN.20 


32  MORPHOLOGY  OF  ANGIOSPERMS 

The  development  of  the  microsporangia  began  to  be  de- 
scribed by  Xa'geli  2  in  1842,  and  was  continued  by  Hofmeister  3 
in  1859-' 61 ;  but  the  first  detailed  account  from  the  standpoint 
of  modern  morphology  is  that  of  Warming  8  in  1873,  which  has 
been  made  the  basis  of  all  subsequent  accounts.  This  was  sup- 
plemented in  1876  by  Engler,9  and  since  then  numerous  inves- 
tigators have  added  extensively  to  the  literature  of  the  subject. 

The  anther  at  first  is  a  homogeneous  mass  of  small  meriste- 
matic  cells  covered  by  an  epidermis  (Fig.  9).  Very  early  it 


FIG.  9. — Development  of  the  microsporangium.  A-D,  Doronicum  macrophyllum :  A, 
transverse  section  of  very  young  anther,  showing  primary  sporogenous  cell  (a)  and 
primary  parietal  cell  (b) ;  _Z?,  slightly  older  stage ;  6y,  longitudinal  section  of  anther  in 
same  stage  as  that  shown  in  B  \  I),  later  stage ;  a,  sporogenous  cells.  E,  Menyanthes 
trifoliata,  transverse  section  of  a  microsporangium  at  a  still  later  stage  showing 
tapetum  (t)  and  microspore  mother-cells  (sm).  F,  Mentha  aquatica,  transverse  sec- 
tion showing  tapetum  (t}  and  sporogenous  cells  (a). — After  WARMING,  from  Goebel's 
Outlines  of  Classification  and  Special  Morphology. 

becomes  faintly  four-lobed  in  cross-section,  and  the  differentia- 
tion of  the  vascular  strand  of  the  connective  outlines  the  gen- 
eral plan  of  the  structure.  The  whole  hypodermal  layer  of 
cells,  representing  the  outermost  layer  of  the  periblem,  is  prob- 
ably to  be  regarded  as  archesporial  in  its  possibilities,  and  one 
region  of  it  is  just  as  likely  as  another,  under  similar  condi- 
tions, to  develop  into  actual  archesporial  cells.  The  favorable 
conditions  for  this  development,  however,  are  under  the  lobes ; 
so  that  almost  simultaneously  with  their  appearance,  a  plate 


THE  MICROSPORAXGIUM  33 

of  hypodermal  cells  becomes  differentiated  in  each  lobe,  dis- 
tinguished from  the  adjacent  cells  by  their  larger  size,  their 
usual  radial  elongation,  their  larger  nuclei,  and  their  different 
reaction  to  stains.  In  cross-section  this  plate  is  a  single  row  of 
cells  of  variable  number,  sometimes  almost  equaling  in  extent 
the  contour  of  the  lobe,  as  in  Mentha  aquatica  (Warming8)  ; 
sometimes  consisting  of  four  to  six  cells,  as  in  Orchis  maculata 
(Guignard  10) ;  sometimes  three  or  four  cells,  as  in  Hemerocal- 
Us  fulva  (Fullmer  24)  ;  sometimes  one  or  two  cells,  as  in  Conval- 
laria  majalis  and  Potamogeton  foliosus  (Wiegand 25) ;  and 
sometimes  constantly  one  cell,  as  long  known  in  Malvaceae  and 
most  Compositae,  and  recently  reported  in  Avena  fatua  by  Can- 
non.26 In  longitudinal  section  the  plate  extends  approxi- 
mately the  length  of  the  anther,  being  a  single  row  of  cells 
in  case  the  cross-section  consists  of  a  single  cell;  but  in  Mimo- 
seae  .the  whole  archesporium  is  reported  by  Rosanoff  4  as  being  a 
single  cell,  as  is  also  the  case  in  Euphorbia  corollata,  as  re- 
ported by  Miss  Lyon.22  The  general  fact  becomes  clear,  there- 
fore, that  an  exceedingly  variable  amount  of  the  hvpodermal 
layer  may  become  archesporium,  from  nearly  all  of  it  to  a  single 
cell ;  and  further,  that  this  amount  usually  varies  within  cer- 
tain limits  in  the  same  species,  and  that  the  extent  of  the 
archesporium  is  in  no  way  related  to  the  primitive  or  highly 
specialized  character  of  plant  groups. 

The  subsequent  divisions  to  the  mother-cell  stage  usually 
follow  one  another  rapidly  (Fig.  10).  Following  the  history 
of  a  single  sporangium,  the  radially  elongated  archesporial  cells 
all  divide  equally  and  almost  simultaneously  by  periclinal  walls, 
forming  an  outer  layer  (primary  parietal,*  Fig.  9,  A,  b)  and 
an  inner  layer  (primary  sporogenous,f  Figs.  9,  A,  a,  and  10, 

*  This  has  been  commonly  called  the  "primary  tapetal  layer,"  on  the 
ground  that  the  tapetum  is  one  of  its  derivatives.  At  most  only  a  part  of  the 
tapetum  can  be  derived  from  it,  and  in  some  cases  none  of  the  tapetum  is  so 
derived.  Besides,  the  tapetum  is  a  physiological  layer  of  variable  morpho- 
logical origin.  The  essential  morphological  feature  of  this  outer  sterile  layer 
is  that  it  develops  the  wall  of  the  embedded  sporangium,  and  hence  we  have 
preferred  to  designate  it  as  the  primary  parietal  layer. 

f  This  is  the  "archesporium"  of  Goebel's  Outlines  of  Classification  and  of 
other  texts.  With  such  an  application  of  the  term  the  archesporium  of  the 
mierosporangium  of  Angiosperms  does  not  homologize  with  that  of  the  mega- 
sporangium,  and  is  of  indefinite  application  among  the  PterMjMfcytes.  By 


34  MORPHOLOGY  OF  ANGIOSPERMS 

A).  The  names  used  to  designate  these  two  layers  indicate 
their  subsequent  history,  the  former  producing  the  wall  of  the 
t  embedded  sporangium,  and  the  latter  the  sporogenous  tissue. 

The  cells  of  the  primary  parietal  layer  divide  by  periclinal 
walls,  so  that  usually  a  definite  series  of  concentric  parietal 
layers  appears  (Fig.  8,  A).  Walls  in  other  directions  also  ex- 
tend the  parietal  layers  uniformly  with  the  rapidly  enlarging 
anther.  The  number  of  parietal  layers  is  variable,  but  in  most 
cases  there  are  from  three  to  five.  Sometimes  there  are  only  two 
layers,  as  inSilpJiium  (Merrell  2S)  and  in  Quercus  (Conrad  29)  ; 
and  among  the  Poritederiaceae  Smith  21  has  regularly  found  six. 
Even  higher  numbers  have  been  reported,  and  Goebel  u  (p. 
368)  cites  Agave  americana  as  developing  eight  to  twelve 
fibrous  or  endothecial  layers.  In  Rhopalocnemis  phalloides 
(Balanophoraceae)  Lotsy 30  has  shown  that  the  sporangia  of 
the  curious  axial  stamen  do  not  organize  definite  parietal  layers 
and  have  no  method  of  dehiscence,  although  the  microspores 
are  fully  matured. 

The  outermost  parietal  layer  usually  develops  very  differ- 
ently from  the  others,  and  has  been  called  the  "  endothecium." 
This  name  was  given  by  Purkinje  l  to  designate  all  the  layers 
of  the  dehiscing  anther  wall  within  the  epidermis,  which  latter 
he  named  the  "  exothecium."  Since  in  most  cases  the  outer- 
most parietal  layer  is  the  only  one  represented  in  Purkinje's 
"  endothecium,"  the  name  has  come  to  be  restricted  to  it,  which 
seems  to  us  unfortunate,  for  it  should  be  retained  in  its  original 
application  and  used  only  in  connection  with  the  dehiscing 
anther-wall.  It  remains  true,  however,  that  the  outermost  pa- 
rietal layer  generally  becomes  the  endothecium,  and  in  the  fol- 
lowing account  this  condition  will  be  presented.  If  the  anther 
does  not  dehisce,  the  endothecial  cells  do  not  become  specially 
modified ;  but  if  the  anther  dehisces,  the  cells  develop  thicken- 
ing bands  in  various  ways,  the  position  and  extent  of  these 
banded  cells  being  directly  related  to  the  method  of  dehiscence 
(Fig.  7). 

Between  the  outermost  and  innermost  parietal  layers  there 
are  usually  one  to  three  "  middle  layers,"  and  this  amount  of 

applying  the  term  to  the  first  cell  or  group  of  cells  differentiated  from  the 
ordinary  vegetative  cells  to  produce  sporogenous  tissue,  it  is  easy  of  applica- 
tion and  the  homologies  are  definite. 


FIG.  10. — SilpMum  integrifolium.  Longitudinal  sections  of  microsporangia ;  x  520. 
/(,  single  row  of  archesporial  cells  ;  in  two  cells  division  into  primary  sporogenous 
and  primary  parietal  cells  has  already  taken  place.  B,  sporogenous  and  tapetal  cells 
sharply  differentiated.  £7,  later  stage  showing  spore  mother-cells  in  synapsis.  Z>, 
a  tetrad  (only  three  microspores  shown)  formed  within  the  spore  mother-cell.— After 

MERRELL.28 

35 


36 


MORPHOLOGY  OF  ANGIOSPERMS 


variation  may  occur  in  the  same  wall,  as  noted  by  Coulter  19 
in  Ranunculus.  The  cells  of  these  layers  are  usually  tabular, 
and  gradually  become  flattened  and  disorganized;  but  in  some 
cases  the  one  or  two  innermost  middle  layers  become  prominent 
as  a  part  of  the  tapetum ;  in  others  the  outer  ones  may  become 
a  part  of  the  endothecium;  and  occasionally  there  is  no  dis- 
organization of  parietal  layers. 

The  innermost  parietal  layer,  as  a  rule,  becomes  part  of  the 
tapetum,  which  is  a  jacket  of  nourishing  cells  in  immediate  con- 
tact with  the  sporogenous  tissue  (Figs.  9,  10).  The  tapetum  has 


FIG.  IV. — Zostera  marina.  A,  young  microsporangium  with  archesporial  cells  shaded. 
B,  later  stage  showing  tapetum  derived  from  sporogenous  cells ;  tf,  tapetum ;  p,  pollen 
mother-cells ;  st,  sterile  cells,  as  shown  by  transverse  wall.  C,  portions  of  the  two 
long  cells  resulting  from  the  first  division  of  the  pollen  mother-cell.  D.  portion 
of  a  microspore  showing  the  nuclear  division  that  gives  rise  to  the  generative 
and  tube  nuclei ;  there  are  six  chromosomes.  E,  the  filiform  pollen  grain. — After 

KOSENBERG.83 


no  definite  morphological  boundary  or  origin,  but  results  from 
pressing  into  special  physiological  service  the  sterile  cells,  of 
whatever  origin,  contiguous  to  the  sporogenous  tissue.  While  one 


THE  MICROSPORANGIUM 


37 


FIG.  12. — Lemna  minor.  Section  of  microspo- 
rangium  showing  some  of  the  spore  mother- 
cells  broken  down  and  functioning  as  tape- 
turn  :  x  1100. — After  CALDWELL.SS 


layer  of  cells  is  the  rule,  the  tapetum  may  include  two  or  more 
layers,  as  pointed  out  by  Frye  33  in  Asclepias.  The  same  inves- 
tigator has  also  followed  the  origin  of  that  portion  of  the  tape- 
tum next  the  connective 
from  the  plate  of  cells  im- 
mediately within  the  arche- 
sporium;  and  in  a  recent 
paper  Rosenberg 32  de- 
scribes and  figures  the 
much  elongated  archespo- 
rial  cells  of  Zostera  as  cut- 
ting off  isodiametric  cells 
at  each  end,  that  divide 
more  or  less  and  form  the 
tapetum  on  the  outer  and 
inner  surfaces  of  the  spo- 
rogenous  mass  (Fig.  11, 
B,  t).  There  is  evidence, 
therefore,  that  in  certain 
cases  the  tapetum,  or  at  least  part  of  it,  may  be  derived 
from  sterile  cells  cut  off  from  the  periphery  of  the  sporog- 
enous  mass.  Such  a  probability  is  also  reported  by  Coul- 
ter 19  in  Ranunculus,  and  by  Webb 34  in  Astilbe.  Enough 
is  known,  at  least,  to  lead  to  the  conclusion  that  any  sterile 
cells  in  contact  with  the  sporogenous  tissue  assume  the  tape- 
tal  function.  This  is  a  well-known  fact  in  connection  with 
sterile  mother-cells,  which  in  this  sense  are  a  part  of  the  tape- 
tum. Among  the  Pontederiaceae  Smith 21  found  that  the 
tapetal  cells,  closely  adherent  to  the  mother-cells,  are  often 
wedged  among  them ;  and  in  Lemna  Caldwell  23  observed  that 
the  cells  of  the  regular  tapetal  jacket  often  divide  and  form 
groups  of  cells  projecting  deep  among  the  mother-cells,  sterile 
mother-cells  also  disintegrating  (Fig.  12)  ;  while  in  Symplo- 
carpus  Duggar  27  reports  that  the  tapetal  cells  become  free  and 
"  wander  "  among  the  mother-cells.  It  seems  clear,  therefore, 
that  the  tapetum  is  a  set  of  sterile  cells  that  nourish  the  func- 
tioning mother-cells,  and  that  while  ordinarily  it  is  a  definite 
layer  none  of  which  is  derived  from  the  primary  sporogenous 
cells,  it  may  include  a  variety  of  morphological  elements. 
As  a  rule,  the  complete  organization  of  the  tapetal  jacket  is- 


38 


MORPHOLOGY  OF  ANGIOSPERMS 


D 


coincident  with  the  mother-cell  stage,  but  the  greatest  devel- 
opment of  the  tapetal  cells  is  during  the  formation  of  tetrads. 
During  this  process  they  may  increase  greatly  in  size,  this  being 
associated  with  the  disorganization  of  the  cells  of  one  or  more 
of  the  middle  layers.  It  is  very  common  for  the  enlarged 
tapetal  cells,  filled  with  food  material,  to  become  binucleate 
(Fig.  10,  (7),  and  later  even  multinucleate,  as  in  Typha  (Schaff- 

ner17)  and  Hepatica  (Coul- 
ter19), in  the  latter  genus 
six  to  thirteen  nuclei  hav- 
ing been  observed  in  a  sin- 
gle cell.  At  the  end  of  the 
tetrad  division  the  tapetal 
cells  usually  become  disor- 
ganized, also  such  of  the 
middle  layers  as  have  not 
disorganized  previously,  and 
the  outermost  parietal  layer 
begins  to  develop  the  thick- 
enings characteristic  of  the 
endothecium.  The  fact  that 
the  endothecium  may  con- 
sist of  additional  layers  of 
cells  has  already  been  men- 
tioned. 

During  the  development 
of  the  parietal  layers  the 
primary  sporogenous  cells 
either  directly  or  by  divi- 
sion produce  the  mother- 
cells.  When  division  oc- 
curs, it  is  in  every  direc- 
tion, so  that  all  appearance 
of  layers  is  lost.  Perhaps 

the  usual  case  is  for  the  primary  sporogenous  cells  to  divide  two 
or  three  times,  but  there  are  sometimes  more  divisions,  and  a 
number  of  cases  are  known  in  which  the  primary  sporogenous 
cells,  without  division,  become  mother-cells,  as  has  been  long 
known  in  Malva,  Datura,  Mentha,  and  Chrysanthemum,  and 
recently  reported  for  several  species  of  Asclepiadaceae  by  Stras- 


FIG.  13. — A  and  Z>,  Orchis  maculata :  A,  trans- 
verse section  of  an  anther  with  four  micro- 
sporangia,  each  showing  five  or  six  cells, 
each  of  which  gives  rise  to  a  "  massula  "  as 
shown  in  D.  B,  C,  and  E,  Neottia  ovata: 
B,  a  tetrad ;  C,  the  four  raicrospores  within 
the  common  wall  dividing  to  form  tube  nu- 
cleus and  generative  cell ;  E,  the  division 
completed ;  two  of  the  microspores  show  the 
generative  cell  cut  off  by  a  lenticular  wall. 
A  x  25 ;  D  x  240 ;  B,  <7,  E  x  365.— After 

GUIONABD.10 


THE  MICROSPORAXGIUM  39 

burger  31  and  by  Frye.33  The  case  of  certain  orchids,  such  as 
Orchis  maculata,  Calanthe  ve rat ri folia,  and  Neottia  ovata,  in- 
vestigated by  Guignard,10  and  their  allied  forms,  deserve  special 
mention.  Each  primary  sporogenous  cell  gives  rise  to  a  well- 
defined  mass  of  mother-cells  known  as  a  massula  (Fig.  13,  A, 
D),  and  separated  from  its  fellows  by  thicker  walls. 

The  mother-cells  and  their  nuclei  usually  increase  very 
much  in  size,  and  differ  from  the  adjacent  cells  in  their  reaction 
to  stains.  This  growth  is  usually  accompanied  by  a  rounding 
•of  the  cells  and  their  separation  from  one  another,  and  also  by 
a  thickening  of  the  wall;  but  in  many  Dicotyledons  (Tropaeo- 
lum,  Althaea,  etc.)  the  mother-cells  do  not  become  isolated,  and 
remain  packed  closely  together  in  the  sporangium,  due  probably 
to  the  tardy  disorganization  of  the  tapetum  or  its  failure  to 
disorganize. 

The  time  relations  of  the  events  described  to  those  that  form 
the  history  of  the  corresponding  megasporangium  are  exceed- 
ingly variable,  but  the  case  of  Astilbe,  as  described  by  Webb,34 
may  be  taken  as  an  illustration,  especially  as  it  probably  rep- 
resents an  average  case.  The  microsporangia  develop  rapidly, 
maturing  in  one  or  two  weeks,  and  precede  the  megasporangia 
.stage  for  stage.  The  anthers  are  rounded  and  enlarged  before 
the  carpellary  cavity  is  closed  over;  the  four  microsporangia 
are  well  marked  when  the  "  placentae  "  are  wholly  undiffer- 
•entiated ;  the  tapetum  is  organized  and  the  mother-cell  stage 
reached  when  the  integuments  have  not  appeared;  during  the 
tetrad  stage  the  integuments  appear,  while  the  microspores  are 
'"  rounded  off  "  before  the  functional  niegaspore  is  determined. 
The  most  extreme  cases  are  probably  certain  orchids  in  which 
pollination  occurs  before  ovules  are  formed;  and  oaks  (Con- 
rad29), in  which  pollination  occurs  one  spring  and  the  ovules 
do  not  develop  until  the  next. 

The  case  of  Lemna,  as  reported  by  Caldwell,23  deserves  sepa- 
rate mention  (Fig.  14).  In  the  nascent  anther  a  single  hypo- 
dermal  group  of  cells  appears  as  an  archesporium  and  enters 
upon  the  usual  history,  a  wall  of  several  layers  and  a  broad  spo- 
rogenous mass  being  formed.  A  plate  of  sterile  cells  gradually 
divides  this  sporogenous  mass  into  two,  each  of  which  continues 
to  divide  as  the  anther  increases  in  size.  Each  of  these  two 
.sporogenous  masses  is  divided  by  a  plate  of  sterile  cells,  so  that 


40  MORPHOLOGY  OF  ANGIOSPERMS 

four  distinct  sporogenous  groups  are  formed,  each  surrounded 
by  its  own  tapetum.  As  a  result,  the  mature  anther  seems  to 
contain  the  usual  four  sporangia.  Such  a  case  makes  the  defi- 
nition of  a  sporangium  difficult.  If  a  single  archesporium  is 
the  criterion,  Lemna  has  a  single  sporangium;  if  a  group  of 
mother-cells  invested  by  a  tapetum  is  the  criterion,  it  has  four 
sporangia.  The  explanation  probably  lies  in  the  fact  that  the 
whole  outer  layer  of  the  periblem  is  capable  of  becoming  trans- 


FIG.  14. — Lemna  minor.  Development  of  microsporangium  and  sporogenous  tissue.  A 
young  stamen  with  sporogenous  cells.  .Z?,  two  young  stamens ;  in  the  one  at  the 
left  the  sporogenous  tissue  is  becoming  divided  by  a  sterile  plate.  (7,  a  more  ad- 
vanced stage  than  B.  2),  a  single  stamen  showing  the  four  masses  of  sporogenous 
tissue  well  separated  by  sterile  plates.  A  x  1100 ;  B,  C,  D  x  712.— After  CALD- 

WELL.28 

formed  into  an  archesporium,  and  that  while  in  ordinary  cases 
archesporial  tissue  is  developed  in  four  separate  regions,  in 
Lemna  the  conditions  favor  a  more  general  development.  To 
divide  a  large  sporogenous  mass  by  sterile  plates  for  better  nu- 
trition is  too  common  to  call  for  any  special  remark.  As  for 
the  definition  of  a  sporangium,  it  is  probably  not  best  to  define 
it  too  rigidly,  but  to  use  the  term  as  one  of  convenience.  From 


THE  MICROSPORANG1UM  41 

this  standpoint,  there  is  no  objection  to  speaking  of  the 
four  groups  of  mother-cells  in  Lemna  as  four  sporangia,  which 
have  had  quite  an  exceptional  origin.  The  phenomenon  is 
too  unique  as  yet  among  Angiosperms  to  justify  any  generali- 
zation. 

The  growth  of  mother-cells  and  the  enlargement  of  the  spo- 
rangial  cavities  usually  result  in  reducing  to  a  thin  plate  the 
sterile  tissue  separating  the  two  sporangial  cavities  on  each  side 
of  the  anther.  As  dehiscence  approaches,  this  plate  usually 
disappears,  and  the  two  sporangial  cavities  become  fused  into 
a  single  loculus  of  the  anther  (Fig.  7).  In  the  mature  condi- 
tion, therefore,  such  an  anther  contains  two  loculi  or  "  pollen- 
sacs."  While  this  represents  the  ordinary  condition  of  the 
mature  anther,  among  the  Araceae  it  is  reported  that  the  single 
loculus  of  the  anther  is  formed  by  the  fusion  of  four  sporan- 
gial cavities,  and  in  Sassafras  it  is  well  known  that  the  four 
remain  separate.  In  case  an  anther  contains  only  two  sporan- 
gia, as  among  Asclepiadaceae,  there  is  no  fusion,  and  each 
loculus  is  a  single  sporangial  cavity. 

The  mechanism  for  the  dehiscence  of  anthers  is  extremely 
varied  (Fig.  15),  and  needs  much  more  investigation  than  it 
has  received.  By  far  the  most  common  method  is  by  means 
of  a  longitudinal  fissure,  a  definite  stomium  developing,  as  in 
L ilium  (Fig.  7),  and  opening  by  means  of  the  drying  of  the 
anther-walls,  the  contraction  of  the  epidermal  cells  being 
greater  than  that  of  the  endothecial  cells  with  their  thick  bands. 
There  is  also  dehiscence  by  a  short  apical  fissure,  as  in  Solanum 
and  certain  Ericaceae ;  by  a  terminal  pore,  formed  by  the  dis- 
organization of  a  small  portion  of  tissue,  as  in  certain  Erica- 
ceae ;  by  hinged  valves,  as  in  Berberis,  Sassafras,  and  Hama- 
melis ;  and  by  irregular  breaking  and  exfoliating  of  superficial 
tissues,  as  in  the  axial  stamens  of  Naias.  The  details  of  these 
methods,  and  of  others,  should  be  investigated  from  the  stand- 
point of  the  development  of  the  mechanism,  for  such  as  we  have 
are  too  vague  and  superficial  to  be  of  much  significance. 

The  mother-cell  stage  of  the  microsporangium  is  regarded 
as  the  end  of  the  history  of  the  sporophyte  in  this  direction, 
chiefly  because  the  division  of  the  mother-cell,  preceded  by  a 
more  or  less  prolonged  rest,  is  a  reduction  division,  and  in  con- 
sequence the  resulting  cells  have  the  feature  most  characteristic 


42  MORPHOLOGY  OF  ANGIOSPERMS 

of  gametophytic  tissue — namehythe  reduce'd  number  of  chromo- 
somes (Fig.  53).  With  this  division,  therefore,  the  history  of 
the  male  gametophyte  begins.  This  line  of  demarcation  be- 
tween sporophyte  and  gametophyte  is  easy  to  define,  but  does 


FIG.  15. — Forms  of  stamens,  1,  Calandrinia  compressa  ;  2,  Solanum  Lycopersicum ;  3, 
Galanthus  nivalis;  4,  Cyclamen  europaeum\  5,  Ramondia  pyrenaica;  6,  7,  Cassia 
lenitiva ;  8,  Pyrola  rotundifolia ;  9,  Arctostaphylos  Uva-ursi  ;  10,  A.  alpina ;  1 J, 
Vaccinium  uliginosum :  12,  Pyrola  uniflora ;  IS,  Medinilla  (after  BAILLON)  ;  H, 
Vaccinium  Oxycoccus ;  15,  Calceolaria  Pavonii ;  16,  Tozzia  alpina ;  17,  18,  Sikbaldia 
procumbens;  19,  Galeopsis  angustifolia;  20,  21,  Erythraea  Centaur eum\  22,  23,  Me- 
lissa officinalis;  2^,  25,  Calla  palustris;  26,  Nyctandra  (after  BAILLON);  27,  28, 
Globularia  cordifolia;  29,  30,  Theobroma  Cacao ;  31,  Pinguicula  vulgaris;  32, 
Garcinia. — From  KERNER'S  Pflanzenleben. 

not  result  in  so  simple  a  conception  of  the  alternating  genera- 
tions as  to  begin  the  gametophyte  with  the  germinating  spore, 
for  it  involves  the  simultaneous  origin  of  four  gametophytic 
generations  from  the  mother-cell  through  an  intermediate  divi- 
sion. The  claim  that  the  reduction  division  must  be  regarded 


THE   MICROSPORANGIUM  43 

as   ushering   in   the   gametophyte   was   first   urged   by    Stras- 
burger,12  whose  paper  closes  as  follows: 

u  The  reduction  in  number  of  the  chromosomes  takes  place, 
among  the  higher  plants,  in  the  mother-cells  of  the  spores,  and 
it  is  consequently  these  which  must  be  regarded  as  the  first 
term  of  the  new  generation.  They  assert  this  their  true  sig- 
nificance in  that  they  usually  isolate  themselves  from  cohesion 
with  other  cells  and  become  independent,  although  this  inde- 
pendence is  only  of  practical  utility  in  the  case  of  the  products 
of  their  division — that  is,  of  the  spores.  Hence  the  center  of 
gravity  of  the  developmental  processes  which  take  place  in  both 
micro-  and  macrosporangia  of  Cryptogams  and  Phanerogams 
does  not  lie  in  those  cells,  cell-rows,  or  cell-aggregates  which 
give  rise  to  the  sporogenous  tissue  and  have  been  designated 
'  archesporium  '  by  Goebel.  The  archesporium  still  belongs 
to  the  sexually  developed  asexual  generation;  it  is  only  the 
spore  mother-cells  which  initiate  the  new  sexual  generation; 
consequently  the  presence  or  absence  of  a  well-defined  arche- 
sporium is  not  a  matter  to  which  importance  should  be 
attached." 

LITERATURE   CITED 

1.  PURKIXJE,  J.  E.    De  cellulis  antherarum  fibrosis  nee  nori  de  gra- 

norum   pollinarium  formis  commentatio  phytotomica.     Vrati- 
slaviae.  1830. 

2.  NAGELI,  C.      Zur  Entwicklungsgeschichte  des  Pollens.     Ziirich. 

1842. 

3.  HOFMEISTER,  W.     Xeuere  Beobachtungen  iiber  Embryobildung 

der  Phanerogamen.     Jahrb.   Wiss.   Bot.    1:   82-188.  pis.   7-10. 
1858. 

4.  ROSAXOFF,  S.    Zur  Kenntniss  des  Baues  und  der  Entwicklungs- 

geschichte des  Pollens  der  Mimoseae.    Jahrb.  Wiss.  Bot,  4 :  441- 
450.  pis.  31-32.  1865. 

5.  ROHRBACH,  P.     Die  Samenknospe  der  Typhaceen.    Bot.  Zeit.  27 : 

479-480.  1869. 

6.  KAUFFMAXN,  N.    Ueber  die  mannlichen  Bliithe  von  Casuarina 

quadrh-ah-is.    Bull.  Soc.  Nat.  Moscou  41 :  374-382.  1869. 

7.  MAGNUS,  P.     Zur  Morphologic  der  Gattung  Naias  L.    Bot.  Zeit. 

27 :   769-773.    1869.    Also  Beitrage  zur  Kenntniss  der  Gattung 
Xaias~L.    Berlin.  1870. 

8.  WARMING.   E.     Untersuchungen  liber  pollenbildende  Phyllome 

und  Kaulome.     Hanstein's  Bot.   Abhandl.   2:    1-90.   pis.   1-6. 
1873. 


44:  MORPHOLOGY  OF  ANGIOSPERMS 

9.  ENGLER,   A.     Beitrage  zur  Kenntniss  der  Antherenbildung  der 
Metaspermen.     Jahrb.  Wiss.  Bot.  10  :   275-316.  pis.  20-24.  1876. 

10.  GUIGNARD,  L.     Recherches  sur  la  developpement  de  1'anthere  et 

du  pollen  des  Orchidees.     Ann.  Sci.  Nat.  Bot.  VI.  14:   26-45. 
pi.  2.  1882. 

11.  GOEBEL,  C.     Outlines  of  Classification  and  Special  Morphology. 

English  translation.  1887. 

12.  STRASBURGER,  E.     The  Periodic  Reduction  of  Chromosomes  in 

Living  Organisms.     Annals  of  Botany  8 :  281-316.  1894. 

13.  VAN  TIEGHEM,  PH.  :  Observations  sur  la  structure  et  la  dehiscence 

des  antheres  des  Loranthacees,  etc.     Bull.  Soc.  Bot.  France  42 : 
363-368.  1895. 

14.  SMITH,  ARMA.    Abortive  Flower  Buds  of  Trillium.    Bot.  Gazette 

22:  402-403.  1896. 

15.  CAMPBELL,  D.  H.     A  Morphological  Study  of  Naias  and  Zanni- 

chellia.     Proc.  Calif.  Acad.  Sci.  III.  1 :  1-62.  pis.  1-5.  1897. 

16.  CHAMBERLAIN,  C.  J.    Contribution  to  the  Life  History  of  Salix. 

Bot.  Gazette  23 :  147-179.  pis.  12-18.  1897. 

17.  SCHAFFNER,  J.  H.    The  Development  of  the  Stamens  and  Carpels 

of  Typha  latifolia.    Bot.  Gazette  24 :  93-102.  pis.  4-6.  1897. 

18.  CAMPBELL,  D.  H.    The  Development  of  the  Flower  and  Embryo 

in  Lilaea  subulata  H  B  K.   Annals  of  Botany  12 :  1-28.  pis.  1-3. 
1898. 

19.  COULTER,  J.  M.     Contribution  to  the  Life  History  of  Ranunculus. 

Bot.  Gazette  25 :  73-88.  pis.  4-7.  1898. 

20.  CHAMBERLAIN,  C.  J.     Winter  Characters  of  Certain  Sporangia. 

Bot.  Gazette  25 :  124-128.  pi.  11.  1898. 

21.  SMITH,  R.  W.    A  Contribution  to  the  Life  History  of  the  Ponte- 

deriaceae.    Bot.  Gazette  25 :  324-337.  pis.  19-20.  1898. 

22.  LYON,  FLORENCE  M.     A  Contribution  to  the  Life  History  of 

Euphorbia  corollata.     Bot,   Gazette   25:    418-426.  pis.  22-24. 
1898. 

23.  CALDWELL,  O.  W.    On  the  Life  History  of  Lemna  minor.    Bot. 

Gazette  27 :  37-66.  figs.  59.  1899. 

24.  FULLMER,  E.  L.    The  Development  of  the  Microsporangia  and 

Microspores  of  Hemerocallis  fulva.     Bot.  Gazette  28 :   81-88. 
pis.  7-8.  1899. 

25.  WIEGAND,  K.  M.     The  Development  of  the  Microsporangium  and 

Microspores  in  Convallaria  and  Potamogeton.     Bot.  Gazette  28: 
328-359.  pis.  24-25.  1899. 

26.  CANNON,  W.  A.   A  Morphological  Study  of  the  Flower  and  Em- 

bryo of  the  Wild  Oat,  Avena  fatua.     Proc.  Calif.  Acad.  Sci. 
III.  1 :  329-364.  pis.  49-53.  1900. 

27.  DUGGAR,  B.  M.     Studies  in  the  Development  of  the  Pollen  Grain 

in  Symplocarpus  foetidus   and   Peltandra  undulata.     Bot. 
Gazette  29 :  81-98.  pis.  1-2.  1900. 


THE  MICROSPORANGIUM  45 

28.  MERRELL,  W.  D.    A  Contribution  to  the  Life  History  of  Silphium. 

Bot.  Gazette  29 :  99-133.  pis.  3-10.  1900. 

29.  CONRAD,  A.  H.    A  Contribution  to  the  Life  History  of  Quercus. 

Bot.  Gazette  29:  408-418.  pis.  28-29.  1900. 

50.  LOTSY,  J.  P.  Rhopalocnemis  phalloides  Jungh.,  a  Morphological- 
systematical  Study.  Ann.  Jard.  Bot.  Buitenzorg  II.  2 :  73-101. 
pis.  3-14.  1900. 

31.  STRASBURGER,  E.    Einige  Bemerkungen  zu  der  Pollenbildung  bei 

Asclepias.    Ber.  Deutsch.  Bot.  Gesell.  19 :  450-461.  pi.  24.  1901. 

32.  ROSENBERG,  0.    Ueber  die  Pollenbildung  von  Zostera.    Meddel. 

Stockholms  Hogsk.  Bot.  Inst.  pp.  21.  1901. 
53.  FRYE,  T.  C.    Development  of  the  Pollen  in  some  Asclepiadaceae. 

Bot.  Gazette  32 :  325-331.  pi.  13.  1901. 
34.  WEBB,  J.  E.     A  Morphological  Study  of  the  Flower  and  Embryo 

of    Spiraea.      Bot.   Gazette    33:    451-460.  figs.  28.    1902.      For 

correction  of  names  see  REHDER  in  Bot.  Gazette  34 :  246,  1902. 
.35.  SHOEMAKER,  D.  N.     Notes  on  the  Development  of  Hamamelis 

virginiana  L.    Johns  Hopkins  Univ.  Circ.  21 :  86-87.  1902. 


CHAPTEK    IV 

THE   MEGASPORANGIUM 

THE  megasporangium,  just  as  the  microsporangium,  is  hy- 
podermal  in  origin,  being  derived  from  the  outermost  layer  of 
the  periblem.  Although  strictly  an  embedded  organ,  it  becomes 
superficially  very  distinct  through  the  growth  of  cells  beneath 
and  around  it,  the  whole  structure  constituting  the  ovule.  Al- 
though in  a  strict  morphological  sense  the  ovule  is  more  than  a 
megasporangium,  just  as  the  ordinary  anther  is  more  than  four 
microsporangia,  the  distinction  is  theoretical  rather  than  prac- 
tical, and  in  the  following  discussion  will  be  disregarded. 

Although  the  carpels  are  concerned  in  forming  all  or  a  part 
of  the  encasement  of  the  ovules,  they  do  not  always  produce 
them.  Just  as  in  the  case  of  the  microsporangia,  and  in  the 
same  sense,  there  are  cauline  as  well  as  foliar  ovules,  and  the 
former  are  much  more  common  than  are  cauline  microsporan- 
gia. This  is  probably  due  to  the  fact  that  the  ovules  are  much 
more  closely  associated  with  the  growing  point  of  the  axis  than 
are  the  microsporangia,  and  hence  the  former  are  much  more 
likely  to  be  borne  by  a  lateral  member  than  the  latter. 

Cauline  ovules  are  either  terminal  or  lateral.  In  the  former 
case  the  apex  of  the  axis  becomes  the  nucellus,  as  is  probably 
true  of  most  orthotropous  ovules,  certainly  in_Naias,  Zanni- 
chellia,  Lilaea,  Piperaceae,  Juglandaceae,  Polygonaceae,  and 
others.  In  the  case  of  laterally  cauline  ovules  apical  growth  of 
the  axis  may  be  checked,  so  that  the  lateral  ovule  appears  to 
arise  in  a  terminal  position  from  the  bottom  of  the  sporangial 
chamber,  as  among  the  Compositae ;  or  the  apical  growth  may 
be  continued  into  the  sporangial  chamber  as  a  dome-shaped 
(Anagallis  arvensis}  or  columnar  (Spergularia  mibra,  Amaran- 
taceae,  etc.)  structure  upon  which  numerous  lateral  ovules  are 
46 


THE  MEGASPORANGIUM 


borne,  giving  rise  to  the  so-called  "  free  central  placentation  " 
of  the  older  botanists.     Cauline  ovules  have  also  been  reported 


c 


D 


FIG.  16. — A,  BalanopJiora  polyandra,  with  archegonium-like  megasporangia ;  x  15. 
J?,  B.  dioica,  a  younger  stage  showing  the  mother-cell  just  after  the  first  division; 
x  200.  <?,  B.  polyandra, "  style  "  with  a  pollen- tube  growing  down  into  the  '•  stylar 
canal";  x  105.  Z>,  B.  dioica,  longitudinal  section  of  a  nearly  ripe  seed;  the  sus- 
pensor  is  not  shown  in  this  section.  E,  a  similar  section  through  the  endosperm, 
and  embryo,  showing  the  suspensor. — After  HOFMEISTER.B 

in  Mijzodendron  punctulatum  by  Johnson,22  and  they  doubtless- 
occnr  in  other  Santalaceae ;  and  in  Sparganium  simplex,  Lilaea, 


f  w  <-•*::  '  ;  ' 


MORPHOLOGY  OF  AKGIOSPEEMS 


subulata,  and  certain  of  the  Araceae  by  Campbell  37)  47'  49  ;  and 
there  is  no  doubt  that  numerous  other  cases  await  discovery. 
It  should  be  remembered  also  that  in  many  cases  of  epigyny  the 

ovules  are  probably  to  be  regard- 
ed as  cauline,  and  if  these  be 
added  to  the  cases  already  indi- 
cated, it  becomes  evident  that 
cauline  ovules  are  exceedingly 
common  and  occur  in  all  grades 
of  Angiosperms. 

In  this  connection  the  curious 
condition  in  Loranthaceae  and 
Balanophoraceae  may  be  consid- 
ered, a  condition  that  may  have 
some  connection  with  their  pecul- 
iar habits.  In  1858  Hofmeis- 
ter  4j  5  studied  various  species  and 
n  outlined  the  prominent  features 

of  these  groups,   describing  and 

PIG.  17. — Balanophora  qlobosa.    >4,nu-      .,,  ,. 

ceiius  with  mother-cell  of  embryo-    illustrating  several  stages  in  the 
sac  (shaded);  the  epidermal  cells    development  of  the  archegonium- 

above  the  mother-cell  give  rise  to  the     like  megasporailgium,  and  also  of 
outgrowth  resembling  the  neck  of  an       , 

archegonium.  £,  later  stage  in  which    the    endosperm    and    embryo    of 
the  mother-cell  has  divided  into  two    Balanophoraceae   (Fig.   16),  and 

cells,  both  of  which  «  very  often  de-     ako  the  puzzling   «  mamelon  "   ill 
velop  into  embryo-sacs";   x  166. — 

After  LOTSY.«    '  Loranthaceae.     Subsequent  inves- 

tigators have  in  the  main  con- 
firmed and  extended  this  work,  the  most  important  modifi- 
cation being  in  the  interpretation  of  the  embryo ;  and  even 
here  Hofmeister's  figures  are  nearly  identical  with  those 
of  the  most  recent  papers  (cf.  Fig.  16  with  Fig.  107).  In 
1882  Treub18  described  the  development  of  the  pistil  of 
Loranthus  sphaerocarpus  (Fig.  19).  A  structure  ("  mame- 
lon ")  arises  from  the  bottom  of  each  of  the  three  or  four 
sporangial  chambers  and  grows  until  it  completely  fills  it, 
and  in  this  structure  hypodermal  archesporia  appear  and 
develop  megaspores  in  the  usual  way.  It  is  a  fair  question 
whether  the  "  mamelon  "  is  a  growth  of  the  axis,  whose  ovules, 
represented  by  separate  archesporia,  are  mechanically  hindered 
from  any  superficial  development;  or  whether  it  is  an  ovule 


THE  MEGASPORANGIUM 


49 


without  an  integument,  in  which  there  are  several  archesporia. 
Hofmeister  favored  the  latter  view,  while  Treub  inclined  to  the 
former,  as  his  explanation  of  it  as  a  fusion  of  rudimentary 
ovules  and  placentas  would  seem  to  indicate.  In  1883  Treub  19 
discovered  exactly  the  same  structure  in  Loranthus  pentandrus. 
In  1895  the  same  investigator  29  described  Balanophora  elon- 
gaia  as  having  no  ovule  or  placenta.  In  1896  this  was  con- 
firmed by  Van  Tieghem 34  for  B.  indica ;  and  in  1899  by 
Lotsy 48  for  B.  globosa  (Fig.  17).  Lotsy  claims  that  in  B. 
globosa  there  are  no  flowers,  carpels,  placenta,  or  ovules;  but 
that  a  hypodermal  cell  in  a  protuberance  of  the  floral  axis  gives 
rise  to  the  embryo-sac,  while 
the  epidermal  cells  over  it  de- 
velop a  long,  style-like  organ 
resembling  the  neck  of  an 
archegonium.  Hofmeister  de- 
scribes and  figures  the  pollen- 
tube  of  B.  polyandra  as  grow- 
ing down  into  this  "  stylar 
canal,"  as  he  called  it  (Fig. 
16,  Cy).  It  would  appear  from 
the  figures  that  the  "  protu- 
berance of  the  floral  axis  "  is 
a  megasporangium  without  in- 
teguments, and  that  the  so- 
called  "  style  "  is  a  remarkable 
outgrowth  of  the  nucellus. 
The  pollen-grains,  as  figured 
by  Hofmeister,  therefore,  come 
in  contact  with  the  nucellus, 
as  in  Gymnosperms.  In  this 
connection  attention  may  be 
called  to  the  remarkable  beak 
developed  by  the  nucellus  of 
Euphorbia  corollata  as  de- 
scribed by  Miss  Lyon  41  (Fig. 
18),  a  beak  which  suggests  the  same  general  tendency  of  the  nu- 
cellus which  has  reached  such  an  extreme  expression  in  Balano- 
phora. The  investigation  of  Rhopalocnemis  phaUoides  (Balano- 
phoraceae)  by  Lotsy,52  however,  as  well  as  the  case  of  Balano- 


FIG.  18.— Euphorbia  corollata.  Longitudi- 
nal section  showing  an  excessive  pro- 
longation of  the  nucellus;  x  650. — After 
LYON.« 


50 


MORPHOLOGY  OF  ANGIOSPERMS 


phora,  suggests  the  explanation.  Lotsy  finds  that  the  enlarged  tip 
of  the  flower  axis  soon  completely  fills  the  cavity  of  the  ovary, 

and  that  one  or  more  hypodermal 
cells  of  this  axis  form  the  mega- 
spores  (Fig.  20).  This  is  exactly 
the  case  of  Loranthus,  and  suggests 
that  in  the  allied  Balanopliora  the 
same  "  mamelon "  is  present,  but 
with  no  carpellary  investment,  the 
naked  nucellus  (as  the  "  mamelon  " 
would  seem  to  be  in  this  case)  de- 
veloping the  remarkable  neck-like 
outgrowth  of  sterile  tissue.  In  both 
families  it  seems  certain  that  the 
megasporangia  are  cauline. 

Foliar  ovules  are  related  to  the 
carpels  in  a  variety  of  ways.  By  far 
the  most  common  position  is  for  the 
ovules  to  arise  in  a  line  along  each 
side  of  one  of  the  two  prominent  vas- 
cular bundles  of  the  carpel,  a  very 
common  position  for  the  sporangia 
of  ferns.  In  the  older  morphology 
this  line  was  thought  to  represent  the 
abutting  margins  of  the  infolded  car- 
pellary leaf,  and  hence  such  ovules 
were  called  "  marginal."  In  fact, 
this  double  line  of  ovules,  and  the 
FIG.  19.— Loranthus  sphaerocarpus.  dehiscence  of  many  carpels  along  it, 

^longitudinal  section  of  a  young      geemed    to    the    Supporters    of    meta- 
flower  showing  the  "  mamelon "  ,  .        _ 

(m);x25.   j;  longitudinal  sec-    morphosis  to  prove  the  foliar  nature 
tion  of  a  "mamelon"  at  a  later    of  the  carpel.     As  might  be  expected 

from  the  behavior  of  sporangia  in 
ferns,  there  are  cases  in  which  ovules 
arise  without  such  close  connection 

with  a  prominent  vascular  bundle.  For  example,  in  Butomus, 
Nymphaea,  Nuphar,  Obolaria,  Bartonia,  and  many  species  of 
Gentiana,  the  ovules  arise  from  the  whole  inner  surface  of  the 
carpel.  In  the  older  terminology  these  were  called  "  super- 
ficial "  ovules,  and  associated  with  them,  curiously  enough,  were 


B 


stage  showing  two  hypodermal 
archesporial  cells ;  x  300. — After 
TBEUB." 


THE  MEGASPORANGIUM 


the  occasional  cases  in  which  the  ovules  arise  from  the  other  vas- 
cular bundle  (the  "  midrib  "  of  the  infolded  leaf  theory),  as  in 
Brasenia,  Cabomba,  and  Astrocarpus  (Eichler,8  2:  17).  Ac- 
cording to  Warming  7  a  third  category  is  necessary  to  include 
such  cases  as  Zannichellia,  Ranunculus,  and  Sedum,  in  which 
he  says  the  ovules  are  "  basal  or  axillary." 

The  general  conclusion  seems  evident  that  ovules  may  arise 
from  any  free  surface  within  the  cavity  of  the  ovary,  whether 
it  be  morphologically  carpel  or  axis;  and  further,  that  if  the 
cavity  of  the  ovary  becomes  obliterated  by  the  enlarged  tip  of 


FIG.  20. — Rhopalocnemis  phalloides.  A,  longitudinal  section  through  the  "mamelon" 
before  the  appearance  of  archesporial  cells.  B,  later  stage  showing  the  two  mega- 
spore  mother-cells  which  develop  directly  into  embryo-sacs,  x  116. — After  LOTST." 

the  axis,  as  probable  in  Loranthaceae  and  Balanophoraceae, 
megasporangia  arise  from  the  hypodermal  cells  of  the  axis 
without  the  definite  organization  of  ovules. 

The  morphological  nature  of  the  ovule  was  much  discussed 
by  the  older  morphologists.  According  to  the  theory  of  meta- 
morphosis it  was  necessary  to  interpret  it  as  a  transformation 
of  some  one  or  more  of  the  vegetative  members.  The  most 
prevalent  view  was  that  it  is  a  transformed  leaf -bud  arising 
from  the  margin  of  the  carpellary  leaf,  as  in  the  well-known 
case  of  Bryophyllum ;  and  Hofmeister  claimed  that  the  ovule 
of  Orchis  is  a  trichome  because  it  arises  from  a  single  epidermal 


52  MORPHOLOGY   OF  ANGIOSPERMS 

cell.  When  cauline  ovules  came  to  notice,  Schleiden,  End- 
licher,  and  others  took  the  extreme  position  that  all  ovules  are 
cauline,  even  those  evidently  parietal  upon  carpels.  This  view 
was  opposed  by  Van  Tieghem,6  Celakovsky,9  and  especially 
by  Warming.10  The  last-mentioned  paper  is  noteworthy  for 
its  presentation  of  the  origin  and  development  of  the  ovule,  as 
well  as  for  its  discussion  of  its  morphology.  These  writers 
maintained  that  the  ovule  is  always  foliar  in  origin,  and  their 
explanations  of  cauline  ovules  are  interesting  on  account  of 
their  ingenuity.  This  view  was  also  maintained  by  Eichler 
in  his  Bluthendiagramme,  where  an  historical  resume  of  the 
whole  subject  may  be  found.  The  most  interesting  feature  of 
the  whole  discussion,  however,  is  the  persistent  idea  that  ovules 
could  not  be  both  foliar  and  cauline.  These  last  observers,  hav- 
ing established  the  foliar  origin,  disproved  the  bud  character 
of  ovules,  since  the  members  of  leaf-buds  arise  in  acropetal 
succession,  while  the  nucellus  and  integuments  are  basipetal. 
It  was  urged  that  the  ovule  is  a  transformed  leaf-lobe  or  leaf- 
outgrowth,  and  that  this  view  homologized  them  with  the  spo- 
rangia of  ferns.  This  was  a  decided  step  in  advance,  and  it 
only  remained  to  abandon  the  doctrine  of  metamorphosis,  and 
to  see  that  the  ovules  (sporangia)  hold  no  necessary  relation  to 
either  leaf  or  stem,  but  are  themselves  long-established  and 
independent  members  of  the  plant  body,  with  a  history  that 
antedates  that  of  either  stem  or  leaf. 

The  length  of  time  from  the  beginning  of  megasporangia  to 
their  maturity  is  very  indefinitely  known,  as  most  investigators 
do  not  seem  to  have  kept  such  a  record.  It  must  be  extremely 
variable,  as  in  the  case  of  the  microsporangia,  and  related  to 
the  seasonal  habit  of  the  plant.  In  Salix  and  Populus  Cham- 
berlain 39  found  that  the  megaspore  mother-cells  are  not  distin- 
guished until  the  renewal  of  growth  in  the  spring,  although  the 
microsporangia  pass  the  winter  in  the  mother-cell  stage;  and 
this  lateness  of  development  may  be  usual  in  the  megaspore 
series.  Enough  cases  have  been  observed,  however,  to  show  that 
a  much  earlier  development  may  often  occur.  For  example,  in 
Acer  rubrum  Mottier 27  discovered  the  mother-cell  stage  in 
March  or  earlier,  the  indication  being  that  this  is  the  winter 
condition ;  Chamberlain  39  found  the  four  megaspores  of  Tril- 
lium recurvalum  fully  formed  early  in  April,  when  the  plants 


THE  MEGASPORANGIUM  53 

were  not  more  than  5  centimeters  high,  and  the  embryo-sac  of 
Hepatica  ready  for  fertilization  while  the  ground  was  still 
frozen;  we  have  seen  embryo-sacs  of  Epigaea  ready  for  fertil- 
ization in  the  autumn,  pollination  probably  occurring  the  fol- 
lowing spring ;  and  Schaffner  56  has  found  that  in  Erythronium 
the  archesporial  cell  begins  to  enlarge  about  the  first  of  October 
and  nuclear  changes  occur,  and  that  by  the  first  of  December  the 
nucleus  is  very  large  and  the  mother-cell  stage  reached,  which 
persists  until  early  spring.  The  subject  should  be  investigated 
especially  in  connection  with  vernal  herbs  and  early  blooming 
shrubs  and  trees. 

The  details  of  the  development  of  the  ovule  have  been  ad- 
mirably given  by  Warming  10  and  Strasburger,13  supplement- 
ing and  correcting  the  earlier  observations  of  Hofmeister,4'  5 
and  the  literature  since  has  grown  so  extensively  that  full  cita- 
tion is  impossible  (Fig.  21).  At  first  the  epidermis  of  the  mem- 
ber upon  which  the  ovule  is  to  appear  is  even,  and  in  the  hypo- 
dermal  layer  the  archesporium  may  or  may  not  be  evident.  A 
slight  protuberance  is  developed  by  cell-divisions,  which  are 
usually  only  radial  in  the  epidermal  layer,  resulting  in  a  more 
extended  plate  of  cells;  but  in  the  hypodermal  layer  they  are 
variable,  resulting  in  a  mass  of  tissue,  or  in  many  cases  in  but 
a  single  axial  row  of  cells.  In  any  event,  the  protuberance 
becomes  more  and  more  prominent  and  constitutes  the  nucellus 
of  the  nascent  ovule. 

After  the  nucellus  has  become  prominent,  an  annular  out- 
growth begins  at  its  base,  and  with  greater  or  less  rapidity 
develops  into  the  inner  and  often  only  integument,  in  most 
cases  overtopping  the  nucellus  (Fig.  3,  7).  In  case  there  is  an 
outer  integument,  its  annular  primordium  becomes  visible  soon 
after  the  inner  integument  is  well  under  way  (Fig.  21).  If  the 
aril  be  placed  in  this  category,  it  has  been  observed  that  this 
third  integument  arises  much  later  than  the  other  two,  usually 
after  fertilization,  as  in  Asphodelus,  Aloe,  Nymphaea,  Podo- 
phyllum,  Euonymus,  Celastrus,  Myristica,  etc.,  although  in  all 
these  cases  its  point  of  origin  does  not  seem  to  be  well  estab- 
lished. Disregarding  the  aril,  two  integuments  seem  to  be  the 
rule  among  Monocotyledons,  the  only  recorded  exception  we 
have  noted  being  Crinum,  although,  doubtless,  there  are  others. 
Two  integuments  prevail  among  the  Archichlamydeae  also,  the 


FIG.  21. — Lilium  pMladelphicum.     A,  ovule  before  the  appearance  of  integuments, 
showing  a  single  hypodermal  archesporial  cell  which  is  also  the  megaspore  mother- 
cell.    J?,  beginning  of  inner  integument.     (7,  beginning  of  outer  integument.    7),  E, 
later  stages.    F,  G,  the  ovule  anatropous  and  the  megaspore  germinating,   x  175. 
54 


THE  MEGASPORANGIOI  55 

tlmbelliferae  being  the  most  notable  exception.  On  the  other 
hand,  a  single  integument  is  characteristic  of  the  ovules  of  the 
Syinpetalae,  as  well  as  of  the  Umbelliferae,  and  some  other 
Archichlamydeae,  such  as  species  of  Ranunculus,  Leguminosae, 
€tc.,  the  integument  being  very  massive  and  in  comparison  with 
the  very  small  nucellus  constituting  the  bulk  of  the  ovule. 
There  seems  to  be  every  indication  that  two  integuments  are 
characteristic  of  the  ovules  of  the  more  primitive  Angiosperms ; 
that  they  persist  among  Monocotyledons  even  among  the  most 
highly  specialized  families ;  but  that  among  Dicotyledons  they 
are  replaced  in  the  higher  groups  by  the  single  massive  integu- 
ment. The  fact  that  the  single  integument  is  more  massive 
even  than  both  integuments  when  there  are  two  suggests  that  it 
represents  two  integuments  in  the  sense  that  their  primordia 
are  no  longer  differentiated.  This  is  very  far  from  meaning 
that  two  integuments  have  fused  to  form  the  single  one,  but 
that  a  single  integument  is  developed  by  the  same  region  that 
in  other  cases  produces  two. 

Certain  exceptional  cases  in  the  development  of  integu- 
ments may  be  noted.  Among  the  Loranthaceae  and  Balano- 
phoraceae  no  integuments  are  formed;  and  the  same  claim  is 
made  by  Chauveaud 24' 65  for  Cynanchum  (Asclepiadaceae), 
perhaps  to  be  explained  by  Asdepias  (Frye66),  in  which  the 
integument  might  be  mistaken  for  part  of  a  naked  nucellus. 
The  same  claim  is  made  for  Santalaceae,  and  it  may  be  true 
of  most  of  them ;  but  in  Myzodendron  punctulatum  Johnson  22 
has  described  a  single-layered  integument  that  does  not  cover 
the  free  end  of  the  embryo-sac.  This  suggests  an  abortion 
of  the  integument,  which  in  other  members  of  the  family 
may  not  have  been  recognized  or  may  even  have  been  sup- 
prcssed.  The  ovule  of  Houstonia  is  said  by  Lloyd  61  to  have 
110  integument.  The  ovule  of  Hippuris  long  had  the  reputation 
of  having  no  integument,  as  reported  by  Schleiden,1  linger,2 
and  Schacht.3  In  1880,  however,  Fischer  15  in  reinvestigating 
it  discovered  that  a  single  integument  is  formed,  but  closes  over 
the  nucellus  so  tightly  as  to  give  the  appearance  of  a  naked 
nucellus.  Oliver 21  discovered  exactly  the  same  behavior  in 
his  new  genus  Trapetta,  except  that  the  integument  is  very 
massive.  The  same  thing  has  also  been  observed  by  Murbeck  57 
in  the  parthenogenetic  AlcJiemilla  alpina,  in  which  the  single 
5 


56 


MORPHOLOGY  OF  ANGIOSPERMS 


integument  so  completely  coalesces  with  the  nucellus  and  closes- 
the  micropyle  that  the  ovule  resembles  a  naked  nucellus.  Zin- 
ger  43  observed  that  the  massive  inner  integument  in  Canna- 
bineae  is  completely  coalescent  with  the  thick  outer  one  over  the 
apex  of  the  nucellus,  and  the  micropylar  canal  becomes  entirely 
closed  by  the  development  of  tissue.  In  cases  of  chalazogamy 
and  persistent  parthenogenesis  such  behavior  of  the  integu- 
ments may  be  expected,  as  well  as  in  other  cases  whose  habits 
do  not  suggest  it. 

In  most  cases,  the  ovule  does  not  merely  become  distinct 
from  the  surface  of  the  member  that  produces  it,  but  is  borne 
upon  a  stalk-like  base  or  funiculus.  It  is  generally  stated  that 


FIG.  22.— Forms  of  ovules  (diagrammatic).  A,  orthotropous ;  B,  anatropous ;  £,  cam- 
py lotropous;  m,  micropyle ;  e,  embryo-sac  ;  n,  nucellus;  c,  chalaza;/,  funiculus. — 
After  PRANTL  in  Engler  and  Prantl's  Nat.  Pflanzenfam. 

the  ovules  of  Gramineae  have  no  funiculus,  but  it  would  be  im- 
possible to  draw  an  exact  line  between  its  presence  and  absence. 
The  direction  of  growth  of  the  ovule  seems  to  be  related 
to  the  orientation  of  the  micropyle  in  reference  to  the  pollen- 
tube.  Mirbel  gave  to  the  resulting  forms  the  names  ortho- 
tropous, campylotropous,  and  anatropous  (Fig.  22).  In  the 
first  case  the  growth  continues  without  the  development  of  any 
curvature,  a  fact  generally  true  of  terminal  cauline  ovules. 
Orthotropous  ovules  are  quite  common,  being  found  among 
Monocotyledons  in  the  Restiaceae,  Eriocaulaceae,  Xyridaceae, 
certain  Araceae,  Commelinaceae,  etc. ;  and  among  Dicotyledons 
in  the  Piperaceae,  Urticaceae,  Polygonaceae,  .Cistaceae,  etc. 
These  are  relatively  primitive  families  of  Monocotyledons  and 
Archichlamydeae,  and  confirm  the  natural  impression  that  th& 


THE  MEGASPORANGIUM  57 

original  angiospermous,  ovules  were  straight.  The  campylotro- 
pous  ovule,  in  which  the  whole  body  of  the  ovule  curves,  is  the 
rarest  type,  among  Monocotyledons  characterizing  the  Grami- 
neae,  Scitamineae,  etc.,  and  among  Dicotyledons  the  Cheno- 
podiaceae,  Caryophyllaceae,  Cruciferae,  Capparidaceae,  Reseda- 
ceae,  etc.  These  families  are  more  or  less  specialized  members 
of  their  alliances,  and  none  of  them  belong  to  the  Sympetalae. 
By  far  the  most  common  form  of  ovule  is  the  anatropous,  and 
although  it  is  extensively  displayed  among  Monocotyledons  and 
Archichlamydeae,  it  is  present  almost  without  exception  among 
the  Sympetalae,  and  may  be  regarded  as  the  most  highly  spe- 
cialized type  of  ovule.  In  its  development  an  anatropous  ovule 
is  at  first  straight  or  nearly  so,  but  very  early  develops  a  curva- 
ture at  a  level  with  the  origin  of  the  first  or  only  integument. 
As  the  integuments  grow  the  curvature  increases,  and  usually 
before  the  outer  integument  is  complete  the  nucellus  is  inverted 
against  the  funiculus  (Fig.  21).  For  this  reason,  in  anatropous 
ovules  with  two  integuments  the  outer  one  is  not  developed  on 
the  side  toward  the  funiculus.  In  abnormal  material  of  Salix 
petiolaris  both  anatropous  and  orthotropous  ovules  have  been 
observed  in  the  same  ovary  (Fig.  6). 

The  archesporium,  as  in  the  microsporangia,  is  recognized 
by  the  increasing  size  and  the  different  reaction  to  stains  of  one 
or  more  hypodermal  cells.  Doubtless  all  of  the  hypodermal 
cells  are  potentially  archesporial,  and  there  is  reason  for  be- 
lieving that  the  deeper  cells  of  the  nucellus,  most  of  which  are 
probably  derivatives  from  the  original  hypodermal  layer,  may 
be  also.  In  the  vast  majority  of  cases,  however,  only  cells  of 
the  hypodermal  layer  show  those  changes  that  are  character- 
istic of  archesporial  cells.  It  is  not  always  easy  to  determine 
just  how  many  hypodermal  cells  are  to  be  included  in  the  ar- 
chesporium,  for  there  is  often  complete  gradation  from  cells 
with  the  size  and  staining  reaction  of  undoubted  archesporial 
cells  to  those  showing  neither  increase  in  size  nor  the  character- 
istic staining  reaction.  This  is  to  be  expected  in  case  all  the 
hypodermal  cells  are  potentially  archesporial,  and  there  is  no 
definite  point  in  its  history  when  such  a  cell  ceases  to  be  merely 
hypodermal  and  becomes  clearly  archesporial.  For  this  reason, 
the  number  of  cells  recorded  as  constituting  the  archesporium 
in  many  plants  can  not  be  regarded  as  precise,  but  as  approxi- 


58 


MORPHOLOGY  OP  AXGIOSPERMS 


mate.  The  prevailing  habit,  however,  is  to  limit  the  arche- 
sporium  to  the  single  hypodermal  cell  that  terminates  the  axial 
row  of  the  nucellus.  This  seems  to  have  resulted  in  the  more 


FIG.  23. — Longitudinal  sections  of  ovules  showing  multicellular  archespcria.  A,  B, 
Astilbejaponica,  x  550;  after  WEBB. «°  (7,  tialix  glaucophylla,  x  600;  after  CHAM- 
BERLAIN-^ Z>,  Rosa  livida,  x  224;  after  STRASBURGER.13  E,  Alchemilla  alpina, 
x  275 ;  after  MURBECK.W  F,  CaUipeltis  cucullaria ;  after  LLOYD.61  <3>  Quercus 
velutina,  x  Y20 ;  after  CONRAD." 

highly  specialized  groups  in  reducing  the  nucellus  within 
the  epidermis  to  this  axial  row,  as  Lilium,  many  Orchida- 
ceae  (Dumee44),  Lobeliaceae  (Marshall-Ward14),  Eubiaceae 
(Lloyd61),  Compositae,  and  many  other  sympetalous  groups. 
In  such  cases  the  nucellus  in  longitudinal  section  shows  only 
three  rows  of  cells. 

It  is  of  interest  to  note  the  recorded  cases  in  which  the 
archesporium  is  said  to  consist  of  more  than  a  single  cell  (Fig. 
23).  In  1879  Strasburger 13  described  the  several-celled  ar- 
chesporium of  Rosa  livida,  and  in  1880  Fischer  15  reported  a 
similar  archesporium  in  Geum,  Sanguisorba,  Agrimonia,  Ru- 


THE  MBGASPORANGIUM 


59 


bus,  and  Cydonia,  indicating  that  this  is  the  prevailing  tend- 
ency among  the  Rosaceae.  In  1882  Guignard  17  added  Erio- 
botrya  to  the  list,  and  in  1901  Murbeck  57  found  an  archesporial 
group  in  Alchemilla  alpina.  Recently,  however,  Pechoutre  63 
has  made  a  general  survey  of  the  Rosaceae,  and  in  all  of  the 
fourteen  genera  studied,  well  distributed  among  the  tribes,  there 
was  found  a  many-celled  archesporium,  showing  a  remarkable 
persistence  of  this  character  throughout  a  large  family.  Among 
the  closely  allied  Saxifragaceae  also,  Webb 60  has  found  in 
Astilbe  this  same  type  of  archesporium. 

In  1891  Treub  23  published  his  account  of  Casuarina,  re- 
porting that  the  archesporium  is  a  group  of  hypodermal  cells, 
and  that  the  derived  sporogenous  tissue  forms  a  large  central 
mass  within  the  nucellus  (Fig.  24).  The  account  and  the  fig- 


D 


FIG.  M.—Casuarina.  Longitudinal  sections  of  nucellus.  A,  section  showing  two  pri- 
mary sporogenous  cells  (shaded) ;  x  190.  j&,  later  stage  showing  extensive  sporog- 
enous tissue:  x  190.  C,  pollen-tube  (with  heavier  walls)  among  the  elongated 
sterile  megaspores ;  x  6k  D.  portion  of  nucellus  at  a  much  earlier  stage  than  £7, 
showing  numerous  megaspore  mother-cells ;  x  157. — After  TREUB.** 

ures  suggest  that  all  of  the  sporogenous  tissue  may  not  be 
derived  from  the  hypodermal  layer.  In  1894  Miss  Benson  28 
discovered  that  a  several-celled  archesporium  is  present  in  Fa- 


60  MORPHOLOGY  OF  ANGIOSPERMS 

gus,  Castanea,  Corylus,  and  Carpinus,  in  the  last-mentioned 
form  finding  a  large  central  mass  of  sporogenous  tissue.  Later, 
Chamberlain  35  found  that  there  are  sometimes  two  or  three 
cells  or  even  six  in  the  archesporium  of  Salix,  and  occasionally 
five  or  six  in  that  of  Populus  tremuloides.  Then  Conrad  53 
described  the  archesporium  of  Quercus  velutina  as  consisting 
of  a  mass  of  twenty  to  sixty  or  even  more  cells,  all  of  which  are 
megaspores  (Fig.  23).  The  archesporia  of  Casuarina,  Car- 
•  pinus,  and  Quercus  are  certainly  not  all  hypodermal,  like  those 
of  the  Rosaceae,  in  which  the  resemblance  to  the  development 
of  the  microsporangia  is  striking.  In  Juglans  cordiformis 
Karsten  64  has  also  found  an  extensive  sporogenous  tissue.  A 
several-celled  or  even  a  many-celled  archesporium,  therefore, 
seems  to  be  a  frequently  expressed  tendency  among  the  Amen- 
tiferae,*  although  it  is  by  no  means  uncommon  among  them 
to  find  the  archesporium  consisting  of  a  single  cell,  as  in  Alnus 
and  Betula. 

Among  the  Ranunculaceae  great  irregularity  in  the  num- 
ber of  archesporial  cells  is  found  even  in  a  single  species. 
Guignard  17  first  found  that  in  Clematis  cirrhosa  the  archespo- 
rium is  sometimes  two-celled ;  and  in  1895  Mottier 30  stated 
that  the  archesporium  of  Delphinium  tricorne  is  sometimes 
more  than  one-celled,  that  of  Ranunculus  abortivus  one  or  two- 
celled,  that  of  Caltlia  palustris  two  to  five-celled,  and  that  of 
Anemonella  thalictroides  probably  many-celled.  Later  Coul- 
ter 38  found  the  archesporial  cells  of  several  species  of  Ranun- 
culus varying  in  number  from  one  to  thirteen  (Fig.  25),  and 
the  several-celled  archesporium  of  Helleborus  cupreus  is  fa- 
miliar. It  is  evident,  therefore,  that  the  Ranunculaceae,  while 
ordinarily  producing  a  one-celled  archesporium,  show  a  strong 
tendency  to  an  increase  in  the  number  of  cells. 

These  three  groups,  Amentiferae,  Ranunculaceae,  and  Rosa- 
•ceae,  are  recognized  as  among  the  more  primitive  members 
of  the  Archichlamydeae,  and  the  temptation  is  strong  to  con- 
clude that  the  many-celled  archesporium  is  a  primitive  feature 
of  the  Dicotyledons.  This  may  be  true  in  a  very  general 
sense,  for  no  large  groups  have  shown  such  a  general  tendency, 
but  account  must  be  taken  of  the  same  phenomenon  in  other 

*  Used  in  this  connection  only  as  a  term  of  convenience  to  include  several 
of  the  more  primitive  orders  of  Archichlamydeae. 


THE  MEGASPORANG1UM 


61 


groups.  Fischer  15  describes  a  several-celled  archesporium  in 
Helianthemum,  Guignard  1T  an  occasional  two-celled  archespo- 
rium in  Capsella,  and  Treub  18  a  two-celled  archesporium  in 
Loranthus  and  one  of  four  or  five  cells  in  Viscum,  while  it  has 
long  been  known  that  Thesium  has  a  several-celled  archespo- 
rium. More  to  the  point,  however,  is  the  occurrence  of  a  several- 
celled  archesporium  among  the  Asclepiadaceae  (Frye  66),  the 
Kubiaceae  (Lloyd  45'  61)  (Fig.  23),  and  the  Compositae.  In  the 
latter  family  Ward  14  describes  an  occasional  archesporium  of 
three  cells  in  Pyrethrum  balsaminatum,  Mottier 26  found  an 
occasional  two-celled  archesporium  in  Senecio  aureus,  and  the 


FIG.  25.— Ranunculus  septentrionalis.  Longitudinal  sections  of  nucellus,  x  400.  A, 
eight-celled  archesporium.  £,  later  stage  showing  germinating  megaspores  with 
two  and  four  nuclei. — After  COULTER.** 

several-celled  archesporium  of  Chrysanthemum  Leucanthemum_ 
is  \vell  known. 

It  is  somewhat  remarkable  that  among  the  Monocotyledons 
there  is  no  record  of  an  archesporium  of  more  than  one  cell 
except  in  the  case  of  Ornithogalum  pyrenqicum,  which  Guig- 
nard17 reports  to  have  an  archesporium  of  two  cells,  only 
one  of  which  gets  beyond  the  archesporial  stage;  and  the  pos- 
sible case  of  Lilium  candidum,  in  which  Bernard  51  reports  two 
embryo-sacs.  We  have  also  seen  two  preparations  of  L.  phila- 
delphicum,  one  showing  three  archesporial  cells  and  the  other 
five. 


62 


MORPHOLOGY  OF  ANGIOSPERMS 


The  archesporial  cells  behave  as  do  those  of  the  microspo- 
rangium, and  in  case  the  archesporium  is  a  plate  of  cells,  the 
resemblance  is  striking.  In  the  large  majority  of  cases,  how- 
ever, the  archesporium  is  a  single  cell,  and  often  by  transverse 
division  it  gives  rise  to  a  primary  parietal  cell  and  a  primary 
sporogenous  cell  (Fig.  26).  That  the  former  cell,  or  plate  of 
cells,  as  it  is  in  the  case  of  a  several-celled  archesporium,  repre- 
sents the  primary  parietal  layer  of  the  microsporangium  seems 

clear.  In  recognition  of  this  fact 
Strasburger  called  it  the  "  tapetal 
cell,"  but  for  reasons  given  under 
the  microsporangium  we  shall  call  it 
the  parietal  cell — that  is,  a  cell  that 
develops  in  part  the  wall  of  the  em- 
bedded sporangium.  Mottier  25  has 
reported  a  very  peculiar  case  in  Ari- 
saema,  in  which  the  single  archespo- 
rial cell  divides  by  anticlinal  walls 
into  three  or  four  cells,  each  of  which 
then  cuts  off  a  parietal  cell.  Just 
how  far  this  is  exceptional  behavior 
remains  to  be  seen,  but  it  intro- 
duces an  interesting  problem  as  to 
the  application  of  the  term  archespo- 
B  rium. 

fiQ.^.—SalixglaucopJiyiia.  Lon-  The    behavior    of    the    primary 

gitudinai  sections  of  nuceiius,    parietal  cell   is   exceedingly  varied. 

x  631.     A,  single  hypodermal       .  .,,.,, 

archesporial  cell  («).   £,  arche-    An  ^  extreme  case  is  for  a  series  of 
sporial  cell  has  given  rise  to  pri-    periclinal  divisions  to  occur,  result- 

rnary  parietal  cell  (t)  and  pri-     j         in   &   }  rQW   of   parietal   cellg 

mary  sporogenous    cell    (m). —  c  . 

After  CHAMBERLAIN.*  corresponding  to  the  parietal  layers 

of   the   microsporangium.      In    case 

there  is  a  plate  of  archesporial  cells  the  radial  rows  of  parietal 
cells  are  very  conspicuous,  as  in  the  Rosaceae  and  many  of  the 
Amentiferae  (Figs.  23,  #,  D,  E).  In  other  cases  the  parietal 
rows  become  lost  by  the  formation  of  anticlinal  walls.  If 
the  mother-cell  broadens  rapidly,  the  first  divisions  of  the  pri- 
mary parietal  cell  may  be  anticlinal,  followed  by  periclinal 
divisions,  as  in  Ruta  graveolens  (Guignard  17)  and  Potamoge- 
ton  foliosus  (Wiegand  54).  The  deep-placing  of  the  sporoge- 


THE  MEGASPORANGIUM  63 

nous  cells  beneath  parietal  tissue  occurs  in  Potamegeton  ("Wie- 
gand,54  Holferty55),  Triticum  (Koernicke  33),  Agraphis 
(Yesque12),  Triylochin  (Vesque12),  Lysichiton  (Campbell47), 
Rosaceae,  Saxifragaceae,  many  Leguminosae  (as  Lupinus,  Cer- 
cis,  Acacia),  Euphorbiaceae,  Cuphea  (Guignard17),  Fuchsia 
(Vesque12),  Mesembrianthemum  (Guignard17),  and  doubtless 
many  other  Monocotyledons  and  Archichlamydeae. 

From  a  conspicuous  development  of  parietal  tissue  there 
is  a  complete  gradation  to  its  entire  suppression.  A  few  peri- 
clinal  divisions  of  the  parietal  cells  may  occur  or  none  at  all. 
Sometimes  in  case  the  periclinal  divisions  have  been  abandoned, 
one  or  more  anticlinal  divisions  may  be  induced  by  the  broad- 
ening of  the  mother-cell,  as  the  single  periclinal  division  in 
Typha  (Schaffner  36)  and  Lemna  (Caldwell  46),  and  the  series 
of  such  divisions  in  Convallaria  (Wiegand 54)  and  Butomus 
(Ward14). 

The  gradation  toward  the  suppression  of  parietal  tissue 
is  further  illustrated  in  cases  where  the  primary  parietal  cell 
divides  or  not  in  the  same  species,  as  in  the  grass  Cornuco- 
piae  (Guignard  17),  Pontederiaceae  (Smith40),  Yucca  (Guig- 
nard  17),  and  Thalictrum  (Overton59).  The  next  stage  is  rep- 
resented by  the  constant  failure  of  the  parietal  cell  to  divide, 
as  in  Alyssum  (Miss  Riddle42)  and  Limnocharis  (Hall58). 
The  last  case  is  of  special  interest  from  the  fact  that  in  the 
cutting  off  of  the  primary  parietal  cell  no  wall  is  formed,  and 
the  cell  speedily  disappears  through  the  growth  of  the  mother- 
cell. 

The  transition  from  an  incomplete  and  ephemeral  primary 
parietal  cell  to  none  at  all  is  natural,  and  this  final  stage,  in 
which  there  is  complete  suppression  of  the  parietal  tissue,  has 
been  reached  by  many  plants.  It  may  be  of  interest  to  consider 
how  far  this  condition  has  been  reached  by  the  great  groups. 

Among  Monocotyledons  the  suppression  of  parietal  tissue 
occurs  in  all  the  higher  families,  but  it  is  usually  associated 
also  with  the  greater  or  less  development  of  this  tissue.  Among 
Gramineae,  Cannon  50  reports  Arena  fatua  as  having  no  parie- 
tal cell,  although  other  Gramineae  are  known  to  possess  it,  and 
in  Triticum  (Koernicke 33)  it  develops  an  extensive  tissue. 
Among  Commelinaceae,  Guignard  17  records  Commelina  stricta 
as  without  a  parietal  cell,  and  Strasburger 13  figures  Trade- 


.64  MORPHOLOGY  OF  ANGIOSPERMS 

scanlia  virginica  as  having  one.  Among  Liliaceae,  Allium, 
Hemerocallis,  Lilium,  Erythronium,  and  Tricyrtis  have  no  pa- 
rietal cell ;  and  Convallaria,  Funkia,  Scilla,  Orniihogalum,  Tril- 
lium, and  Yucca  are  known  to  have  one.  Among  Iridaceae,  the 
only  records  we  have  been  able  to  find  are  those  of  Sisyrinchium 
iridifolium  (Strasburger  13)  and  Iris  slylosa  (Guignard17),  in 
neither  of  which  is  there  a  parietal  cell;  but  it  would  be  very 
unsafe  to  predicate  this  condition  for  the  whole  family.  Among 
the  Cannaceae,  Guignard  17  reports  Canna  indica  as  sometimes 
having  a  parietal  cell  and  sometimes  not,  but  Wiegand  54  finds 
in  it  only  an  abundant  parietal  tissue;  and  the  other  Scitami- 
neae  are  reported  by  Humphrey  32  with  parietal  tissue.  Among 
Orchidaceae,  Gymnadenia  conopsea  (Strasburger13)  and  Or- 
chis pollens  (Goebel,20  p.  391)  were  long  ago  reported  as  with- 
out a  parietal  cell,  but  recently  Dumee,44  examining  a  number 
of  genera  and  species  of  orchids,  reports  them  all  as  having 
parietal  cells.  This  record  probably  fairly  represents  the  con- 
dition of  the  parietal  tissue  among  Monocotyledons.  It  indi- 
-cates  a  general  tendency  to  suppress  it,  which  has  been  success- 
ful in  certain  members  of  the  higher  and  more  specialized 
families. 

Among  the  Archichlamydeae  approximately  the  same  con- 
dition prevails.  The  Ranunculaceae  exhibit  a  surprisingly  uni- 
form suppression  of  the  parietal  tissue,  this  condition  having 
been  found  in  Anemone,  Callha,  Clematis,  Delphinium,  Myo- 
JSUTUS,  and  Ranunculus  (Fig.  27)  ;  while  in  Aquilegia  a  parietal 
cell  may  or  may  not  appear.  Only  Helleborus  (Guignard17) 
and  Thalictrum  (Overton59)  have  thus  far  been  reported  as 
having  a  parietal  cell,  and  this  may  or  may  not  divide.  It  is 
to  be  noted  that  in  Delphinium,  Callha,  and  Jeffersonia  the 
absence  of  parietal  tissue  is  compensated  for  by  numerous  peri- 
•clinal  and  anticlinal  divisions  of  the  overlying  epidermal  cells ; 
and  in  the  Balanophoraceae  this  epidermal  growth  reaches  so 
remarkable  a  development  that  Treub  at  first  called  it  a  style. 
The  same  development  is  seen  in  Hippuris  (Fischer  15),  in  which 
the  apical  epidermal  cell  divides  by  anticlinal  and  periclinal" 
walls  and  forms  a  small,  wedge-shaped  cushion  that  prevents 
the  micropyle  from  being  entirely  obliterated  by  the  closing 
in  of  the  integument.  Among  the  Berber idaceae,  Jeffersonia 
(Andrews31)  has  no  parietal  cell,  and  Mahonia  indica  (Guig- 


THE  MEGASPORANGIUM 

nard 17)  has.  Among  the  Papaveraceae,  Papaver  orientate 
(Vesque12)  has  no  parietal  cell.  Among  Cruciferae,  Capsella 
(Guignard17)  has  no  parietal  cell,  but  Alyssum  (Miss  Kid- 
dle 42)  has  one  that  does  not  divide.  Among  the  Leguminosae, 
Orobus  angustifolius  (Guignard  16)  is  the  only  one  recorded  as 
without  a  parietal  cell;  and  among  the  Umbelliferae,  Sium 
has  no  parietal  cell,  but  in  the  allied  Araliaceae  a  parietal  cell 
is  cut  off  (Ducamp62).  That  Loranthaceae  and  Balanophora- 
ceae  have  no  parietal  tissue  is  probably  only  a  part  of  the  ex- 
tensive modification  of  their  megasporangia.  It  is  perhaps 
noteworthy  that  the  suppression  of  parietal  tissue  among  Ar- 


FIG.  27. — Ranunculus  multifidus.  Longitudinal  sections  of  nucell us,  x  475.  A,  single 
archesporial  cell  (shaded)  which  is  also  the  megaspore  mother-cell,  no  parietal  cell 
being  formed ;  two  of  the  epidermal  cells  above  the  archesporial  cell  show  peri- 
clinal  divisions.  B,  second  division  of  the  megaspore  mother-cell,  by  which  four 
megaspores  are  being  formed. — After  CouLTER.*8 

chichlamydeae  is  most  extensively  displayed  by  the  Ranuncu- 
laceae  and  its  allies,  rather  than  by  the  more  specialized  groups ; 
but  no  generalization  is  safe  until  some  knowledge  of  the  gen- 
eral conditions  among  the  Umbelliferae  and  other  high  groups 
of  the  Archichlamydeae  is  available. 

The  strongest  argument  that  suppression  of  the  parietal 
tissue  of  the  mega  sporangium  is  a  strong  tendency  among  An- 
giosperms  is  that  this  condition  is  universal  among  the  Sym- 
petalae  so  far  as  investigated. 

The  primary  sporogenous  cells  do  not  divide  to  increase 
the  number  of  sporogenous  cells,  so  that  in  the  megasporangium 


66  MORPHOLOGY  OF  ANGIOSPERMS 

of  AngiosjDerms  the  primary  sporogenous  cell  is  the  mother-cell. 
The  only  possible  exception  to  this  is  the  case  of  such  sporog- 
enous masses  as  occur  in  the  ovules  of  Casuarina  ( Treub  23 ) , 
Carpinus  (Miss  Benson28),  and  Quercus  (Conrad53).  If  the 
whole  sporogenous  mass  in  these  forms  is  derived  from  a  hypo- 
dermal  archesporium,  then  of  course  the  primary  sporogenous 
cells  divide  to  form  additional  sporogenous  cells.  But  if  all 
the  sporogenous  tissue  is  an  archesporium,  in  this  case  con- 
tributed to  by  cells  deeper  than  the  hypodermal  layer,  the  pri- 
mary sporogenous  cells  do  not  divide,  nor  do  all  the  archesporial 
cells  give  rise  to  parietal  cells.  In  any  event,  the  cells  of  the 
completed  sporogenous  mass,  whether  archesporial  or  not,  are 
mother-cells. 

The  history  of  the  development  of  the  microsporangia  and 
megasporangia  is  strikingly  similar.  In  both  cases  the  arche- 
sporium is  hypodermal ;  in  the  microsporangium  it  is  usually  a 
plate  of  cells  and  exceptionally  a  single  cell,  while  in  the  mega- 
sporangium  it  is  usually  a  single  cell  and  exceptionally  a  plate 
of  cells.  In  both  each  archesporial  cell  divides  by  a  periclinal 
wall,  cutting  off  a  peripheral  parietal  cell  that  takes  part  in 
developing  a  sporangium  wall  of  a  variable  number  of  layers. 
In  the  development  of  the  megasporangium,  however,  there  is 
a  strong  tendency  to  suppress  the  wall  layers,  probably  as  of 
no  significance  or  even  a  hindrance  in  the  process  of  fertiliza- 
tion. While  in  the  microsporangium  the  primary  sporogenous 
ce,lls  often  divide  a  few  times  before  the  mother-cell  stage  is 
reached,  this  is  by  no  means  always  the  case;  and  although  in 
the  megasporangium  the  primary  sporogenous  cells  usually  do 
not  divide  to  form  mother-cells,  this  is  probably  not  always  true. 
In  both  sporangia  the  mother-cells,  reached  by  the  same 
sequence  of  events,  are  recognized  by  the  fact  that  their  division 
is  the  reduction  division. 

It  is  at  this  point  that  the  history  of  the  megasporangium 
closes,  for  the  reduction  division  is  the  beginning  of  the  female 
gametophyte  (see  p.  41). 

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III.  1 :  329-364.  pis.  49-53.  1900. 

51.  BERNARD,   C.   H.      Recherches    sur    les  spheres  attractives  chez 

Lilium  candidum,  etc.    Jour.  Botanique  14:  118-124,  177-188, 
206-212.  pis.  4-5.  1900. 

52.  LOTSY.  J.  P.    Rhopalocnemis  phalloides  Jungh.,  a  Morphological- 

systematical  Study.    Ann.  Jard.  Bot.  Buitenzorg  II.  2:  73-101. 
pis.  3-14.  1900. 

53.  CONRAD,  A.  H.     A  Contribution  to  the  Life  History  of  Quercus. 

Bot.  Gazette  29:  408-418.  pis.  28-29.  1900. 

54.  WIEGAND,   K.      The   Development  of  the  Embryo-sac   in  some 

Monocotyledonous  Plants..  Bot.   Gazette  30:    25-47.   pis.   6-7. 
1900. 

55.  HOLFERTY,  G.  M.    Ovule  and  Embryo  of  Potamogeton  natans. 

Bot.  Gazette  31 :  339-346.  pis.  2-3.  1901. 

56.  SCHAFFNER,  J.  H.     A  Contribution  to  the  Life  History  and  Cytol- 

ogy of  Erythronium.     Bot.  Gazette  31 :  369-387.  pis.  4-9.  1901. 

57.  MURBECK,  S.    Parthenogenetische  Embryobildung  in  der  Gattung 

Alchemilla.     Lunds  Univ.  Arsskrif t.  36 :   No.  7,  pp.  46.  pis.  6. 
1901 :  Bot.  Zeit.  59 :  129.  1901. 

58.  HALL,  J.  G.    An  Embryological  Study  of  Limnocharis  emargi- 

nata.    Bot.  Gazette  33 :  214-219.  pi.  9.  1902. 


70  MORPHOLOGY  OF  ANGIOSPERMS 

59.  OVERTON,  J.  B.     Parthenogenesis  in   Thalictrum  purpurascens. 

Bot.  Gazette  33 :  363-375.  pis.  12^13.  1902. 

60.  WEBB,  J.  E.    A  Morphological  Study  of  the  Flower  and  Embryo 

of  Spiraea.     Bot.  Gazette  33:  451-460.  figs.  28.  1902.    For  cor- 
rection of  name  see  REHDER  in  Bot.  Gazette  34:  246.  1902. 

61.  LLOYD,  F.  E.     The  Comparative  Embryology  of  the  Rubiaceae. 

Mem.  Torr.  Bot.  Club  8:  27-112.  pis.  8-15.  1902. 

62.  DUCAMP,  L.     Recherches  sur  I'embryogenie  des  Araliacees.    Ann. 

Sci.  Nat.  Bot.  VIII.  15:  311-402.  pis.  6-13.  1902. 

63.  PECHOUTRE,   F.      Contribution  a  1'etude    du    developpement  de 

Tovule  et  de  le  graine  des  Rosacees.    Ann.  Sci.  Nat.  Bot.  VIII. 
16 :  1-158.  figs.  166.  1902. 

64.  KARSTEN,  G.    Ueber  die  Entwicklung  der  weiblichen  Bliithen  bei 

einigen  Juglandaceen.    Flora  90 :  316-333.  pi.  12.  1902. 

65.  CHAUVEAUD,  G.  L.     De  le  reproduction  chez  le  dompte-venin. 

Diss.     Paris.  1902. 

66.  FRYE,  T.  C.    A  Morphological  Study  of  Certain  Asclepiadaceae. 

Bot.  Gazette  34:  389-413.  pis.  13-15.  1902. 


CHAPTER    V 

THE   FEMALE   GAMETOPHYTE 

THE  literature  relating  to  the  female  gametophyte  of  Angio 
sperms  is  so  extensive  that  one  can  not  hope  to  compass  all  of 
its  details.  We  have  selected  for  critical  examination  numerous 
examples,  well  distributed  throughout  the  great  groups,  and  the 
•conclusions  from  these  must  fairly  represent  the  present  state 
of  knowledge.  Even  in  these  cases  it  would  be  hopeless  to 
attempt  the  presentation  of  all  the  details  to  which  attention 
has  been  called,  and  only  those  will  be  considered  that  seem 
most  significant.  There  is  a  prevalent  impression  that  with 
very  few  exceptions  the  history  of  the  female  gametophyte  is 
rigidly  uniform,  but  an  examination  of  the  literature  reveals 
considerable  variation.  This  impression  has  doubtless  arisen 
from  the  fact  that  the  standard  texts  have  almost  uniformly 
selected  a  single  type  of  history  for  description. 

The  important  literature  of  the  subject  dates  from  Hof- 
meister,1'  2  whose  work  was  supplemented  and  corrected  by 
Wanning,3  Vesque,4  Strasburger,5  Fischer,6  Marshall-Ward,8 
Treub  and  Mellink,10  Guignard,11' 12  and  others.  During  the 
last  twenty  years  numerous  investigators  have  added  to  the  lit- 
erature, and  much  of  their  work  will  be  referred  to  later. 

It  was  stated  in  the  previous  chapter  that  we  regard  the 
history  of  the  female  gametophyte  as  beginning  with  the  divi- 
sion of  the  mother-cell.  The  ordinary  product  of  this  division 
is  an  axial  row  of  cells  whose  morphological  nature  was  long 
a  subject  of  discussion  (Figs.  28,  29).  By  many  they  were 
regarded  as  mother-cells  that  do  not  divide,  bui  at  present  there 
is  general  agreement  with  the  view,  stated  by  Overton  28  (p. 
172)  in  1893,  that  they  are  megaspores.  This  means  that  the 
usual  row  of  four  cells  produced  by  the  mother-cell  represents 
6  71 


72 


MORPHOLOGY  OF  ANGIOSPERMS 


the  tetrad  usually  formed  by  the  microspore  mother-cell.     The 
first  mitosis  in  the  megaspore  mother-cell  always  shows  the 


FIG.  28. —  Trillium  recurvatum.  Longitudinal  sections  of  nucellus,  showing  some  early 
stages  in  the  development  of  the  female  gametophyte ;  x  500.  Jl,  megaspore  mother- 
cell  ;  nucleus  shows  six  chromosomes,  the  gametophyte  number.  B,  first  division 
of  nucleus  of  mother-cell.  (7,  second  division  of  nucleus  of  mother-cell ;  mitosis 
nearer  chalaza  much  further  advanced  than  that  at  micropylar  end.  D,  germina- 
tion of  megaspore  nearest  chalaza;  the  other  three  megaspores  represented  only  by 
a  dense,  shapeless  mass. 


THE  FEMALE  GAMETOPHYTE 


73 


reduced  number  of  chromosomes,  and  this  is  true  whether  a  row 
of  two,  three,  or  four  megaspores  is  to  be  produced,  or  the 
mother-cell  is  to  develop  directly  into  the  embryo-sac,  as  in 
L ilium.  In  such  forms  as  Lilium  the  second  mitosis  also  corre- 
sponds in  all  essential  details  with  the  second  division  that  is  to 
result  in  a  row  of  four  megaspores.  The  third  mitosis  differs 


|  FIG.  29. — A,  Canna  indica;  axial  row  of  four  megaspores,  the  innermost  one  beginning 
to  germinate  and  the  other  three  disintegrating ;  after  WiEGAND.80  £,  Eichhornia. 
cra*sipes ;  portion  of  nucellus  showing  four  megaspores,  the  innermost  one  germi- 
nating, and  the  other  three,  which  are  not  separated  by  walls,  disintegrating; 
x  1100 ;  after  SMITH." 

from  the  usual  sporophytic  mitosis  only  in  the  reduced  number 

of  chromosomes  (Miss  Sargant,41  Strasburger,72  Juel88).     Not 

only  do  the  first  two  divisions  agree  in  the  various  types,  but 

they  correspond  minutely  with  the  two  divisions  with  which 

[the  microspore  mother-cell  gives  rise  to  the  tetrad.     That  the 

legaspores  do  not  occur  in  tetrahedral  or  bilateral  arrange- 

lent  does  not  involve  their  morphological  nature,  for  in  the 


MORPHOLOGY  OF  ANGIOSPERMS 


FIG.  30.—  A,  Fatsia  japonica.  Longitudinal 
section  of  nucellus  showing  two  tetrads; 
x!75.  J5,  similar  section  of  AraUa  race- 
mosa,  in  which  the  nucellus  bears  a  strong 

" 


pollen  mother-cells  of  Typha  (Schaffner49)  (Fig.  57)  the 
microspores  are  formed  in  rows  of  four  as  well  as  tetrahedrally, 
while  in  Asclepias  (  Strasburger,96  Frye  "  )  the  microspores 

constantly  appear  in  rows  of 
four  (Fig.  58);  and  in  the 
pollen  mother-cells  of  Zos- 
tera  (Rosenberg93)  the  four 
elongated  microspores  lie 
side  by  side  in  the  same 
plane.  Xor  is  it  a  criterion 
of  a  tetrad  that  all  of  its 
spores  shall  mature,  for  in 

nnrprnriltn  fTnpl  88>>  (V\(? 
59)  only  One  Spore  of  the 
tetrad  functions,  a  habit  to 

»»  observed  also  among  the 
Pteridophytes,  as  in  Mar- 

silea  and  Azolla.  Even  the  rare  case  of  more  than  four  mega- 
spores  in  a  row  is  met  by  the  occasional  occurrence  of  more  than 
four  microspores  in  the  pollen  mother-cells  of  Hemerocallis  fulva 
(Juel,50  Fullmer  65)  and  of  Euphorbia  corollata  (Miss  Lyon  54) 
(Fig.  60).  The  usual  tetrad  arrangement,  however,  is  not  lack- 
ing among  megaspores,  as  observed  by  Ducamp  112  in  Fatsia 
japonica  (Fig.  30),  in  which  after  the  mother-cell  had  divided 
transversely  the  two  daughter-cells  were  observed  to  divide  longi- 
tudinally ;  and  in  one  preparation,  in  which  two  mother-cells  had 
thus  divided,  the  nucellus  looked  very  much  like  an  ordinary  spo- 
rangium. In  another  case  the  middle  cell  of  a  row  of  three  had 
divided  longitudinally.  The  parallel  seems  still  more  striking 
when  microspores  germinate  like  megaspores,  even  reaching  the 
stage  with  eight  free  nuclei,  as  observed  by  Xemec  58  in  the  petal- 
oid  anthers  of  Hyacinthus  orientalis,  whose  microspores  some- 
times show  three  successive  mitoses,  giving  rise  to  four  nuclei  at 
each  end  of  the  pollen-grain  (Fig.  31).  Even  the  formation  of 
three  cells  at  one  end,  and  the  wandering  of  one  polar  nucleus 
toward  the  middle  were  observed,  although  fusion  did  not  occur. 
Nemec  did  not  hesitate  to  homologize  these  divisions  with  those 
occurring  in  the  embryo-sac.  There  seems  to  be  no  longer  any 
reasonable  objection  to  the  view  that  this  row  of  cells,  whose 
formation  is  initiated  by  the  reduction  division,  is  the  homo- 


FEMALE   GAMETOPHYTE 

logue  of  the  tetrad  formed  by  the  microspore  mother-cell.  The 
most  recent  suggestion  as  to  the  nature  of  the  embryo-sac  is  that 
made  by  Atkinson,101  who  claims  that  in  the  ovule  there  do  not 
exist  spores  "  in  the  sense  in  which  they  are  represented  in  the 
Pteridophytes,  or  in  the  microspores  of  the  Spermatophytes," 
but  that  the  angiospermous  embryo-sac  arises  directly  from 
nucellar  tissue  without  the  intervention  of  spores.  As  spores 
are  not  needed  for  distribution  they  are  "  cut  out  of  the  cycle 
of  development,  and  the  embryo-sac  or  gametophyte  arises 
directly  from  the  tissue  of  the  sporophyte." 

In  our  own  judgment  it  seems  clear  that  the  cells  in  question 
are  morphologically  megaspores,  and  if  so  it  would  follow  that 
the  natural  tendency  of  the  megaspore  mother-cell  is  to  form  a 
tetrad.  The  fact  that  the  spores  form  a  row  may  be  due  to  the 


FIG.  %\.—Hyacinthus  orientalis.  Abnormal  germination  of  microspores  in  petaloid 
anthers.  .4,  the  microspore  has  formed  a  sac-like  tube  showing  definite  polarity ; 
B.  a  short  pollen-tube  resembling  an  embryo-sac  at  the  third  nuclear  division ;  the 
heavy  line  below  represents  the  thick  wall  of  the  pollen-grain ;  C,  a  later  stage, 
showing  four  nuclei  at  each  end  of  the  sac-like  pollen-tube. — After  NEMEC.M 

pressure  of  the  surrounding  tissue,  there  being  no  opportunity 
for  early  isolation  and  rounding  off  as  in  microsporangia.  It 
may  be  of  interest  to  note  that  sometimes  after  the  first  divi- 
sion of  the  mother-cell  the  outer  daughter-cell  divides  by  an 
anticlinal  rather  than  a  periclinal  wall,  as  observed  in  Buiomus 


76  MORPHOLOGY  OP  ANGIOSPERMS 

(Marshall-Ward8),  Jeffersonia  (Andrews37),  and  Potamoge- 
ton  (Holferty  9T).  In  the  case  of  Cynomorium  (Juel121),  the 
two  cells  resulting  from  the  first  division  of  the  mother-cell  are 
very  unequal,  the  micropylar  one  being  the  smaller.  This 
smaller  cell  divides  longitudinally  and  the  larger  one  trans- 
versely. Transitions  to  this  condition  in  the  formation  of 
oblique  walls  sometimes  occur,  as  in  Delphinium  (Mottier36). 
The  case  of  Fatsia  japonica  has  been  referred  to  above.  As 
already  indicated,  the  completion  of  a  tetrad  is  by  no  means 
always  attained,  for  there  is  every  gradation  between  a  row 
of  four  megaspores  and  an  undividing  mother-cell  that  func- 
tions directly  as  a  megaspore.  The  explanation  of  this  tend- 
ency to  shorten  the  megaspore  series  is  probably  connected 
with  the  fact  that  only  one  megaspore  of  the  tetrad  functions. 
The  number  of  megaspores  formed  by  the  mother-cell  has  been 
reported  for  very  many  plants,  but  the  records  are  by  no  means 
of  equal  value.  The  reasons  for  this  are  obvious.  One  is  that 
the  sterile  axial  cells  of  the  nucellus  often  simulate  megaspores, 
so  that  too  large  a  number  might  easily  be  reported,  and  great 
care  is  necessary  to  distinguish  them;  and  another  is  that  the 
technique  of  the  earlier  observers  did  not  always  permit  cer- 
tainty. By  far  the  most  important  source  of  inaccuracy,  how- 
ever, is  the  hasty  examination  of  a  great  number  of  forms  by 
a  single  investigator.  Two  megaspores  might  be  reported, 
when  the  same  ovule  collected  a  few  hours  later  might  have 
shown  four  megaspores.  As  a  consequence,  much  of  the  avail- 
able data  can  be  used  only  in  a  very  general  way  as  indicating 
tendencies  of  groups. 

Among  the  Monocotyledons,  about  one-third  of  those  investi- 
gated are  reported  as  forming  complete  tetrads,  in  another 
third  the  mother-cell  does  not  divide,  while  the  remaining  forms 
show  every  intergradation.  Although  one  might  expect  the 
complete  tetrads  to  be  characteristic  of  the  more  primitive 
Monocotyledons,  and  the  undividing  mother-cell  characteristic 
of  the  higher  families,  there  is  as  yet  no  such  evidence,  both 
conditions  occurring  in  all  grades  of  Monocotyledons. 

The  greatest  variability  is  found  among  the  Liliaceae,  possi- 
bly because  more  of  the  species  have  been  investigated  (compare 
Fig.  28  with  Figs.  35  and  36).  For  example,  without  attempt- 
ing to  include  all  the  recorded  cases,  in  Hemerocallis  (Stras- 


THE  FEMALE  GAMETOPHYTE  77 

burger5),  Trillium  (Chamberlain52),  and  Galtonia  (Schnie- 
wind-Thies'95)  four  megaspores  are  reported,  although  in  the 
last  genus  only  two  may  appear;  in  Anthericum  (Strasbur- 
ger5),  and  Tricyrtis  and  Yucca  (Guignard12)  three;  in  Alli- 
um  (Strasburger 5),  and  Agraphis  and  Ornithogalum  (Guig- 
nard12) two;  while  in  Lilium,  Fritillaria,  Furikia,  Tulipa, 
Convallaria  (Wiegand  80),  and  Erythronium  (  Schaffner  98  ) 
the  mother-cell  does  not  divide.  It  may  be  of  interest  to  note 
the  records  of  other  investigators  in  reference  to  some  of  these 
genera.  For  example,  Ikeda  106  reports  four  megaspores  in 
Tricyrtis  hirta,  and  Vesque  4  three  in  Hemerocallis,  Allium, 
.and  Convallaria. 

Among  the  more  primitive  aquatic  families,  Zostera  (Ro- 
senberg92) and  Potamogeton  (Wiegand,66  Holferty97)  have 
three  or  four  megaspores ;  in  Typha  ( Schaffner  49 )  there  is  no 
division  of  the  mother-cell;  and  among  the  Alismaceae,  Alisma 
(Schaffner44)  and  Limnocharis  (Hall109)  have  an  undividing 
mother-cell,  while  Butomus  (AYard8)  has  three  and  sometimes 
four  megaspores. 

Among  the  Gramineae  the  complete  tetrad  is  common 
(Fischer6),  but  Guignard12  reports  only  two  megaspores  in 
Cornucopiae. 

Among  the  Araceae  Mottier  27  reports  two  megaspores  in 
Arisaema,  and  Campbell75  the  same  number  in  Dieffenbachia, 
while  in  the  allied  Lemna  (Caldwell  62)  the  mother-cell  does  not 
divide. 

Among  the  Pontederiaceae  ( Smith  53 )  there  are  four  mega- 
spores, while  Guignard  12  reports  only  two  in  Commelina. 

Among  the  higher  families,  Narcissus  (Guignard 12)  has 
an  undividing  mother-cell;  Iris  (Guignard12)  has  three  mega- 
spores (Vesque  4  reports  four),  and  Tritonia  and  Sisyrinchium 
(Strasburger5)  four;  the  Scitamineae  have  three  or  four, 
excepting  Costus  (Humphrey  40),  in  which  the  mother-cell  does 
not  divide;  while  the  orchids  Gymnadenia  (Strasburger5)  and 
Orchis  (Vesque  4)  have  a  row  of  three  or  four  megaspores. 

That  detailed  study  would  show  that  many  of  these  numbers 
are  not  constant  is  indicated  in  several  instances.  In  Arisaema, 
in  which  two  megaspores  are  customary,  Mottier  27  found  one 
case  in  which  the  transverse  wall  did  not  form,  the  elongated 
mother-cell  appearing  with  a  nucleus  at  each  end ;  while  in  Dief- 


78  MORPHOLOGY  OF  ANGIOSPERMS 

fenbachia,  of  the  same  family,  Campbell  75  states  that  the  inner 
one  of  the  two  cells  may  divide,  forming  a  row  of  three  mega- 
spores.  Among  the  Pontederiaceae,  Smith  53  found  great  varia- 
tion in  the  development  of  the  megaspores.  While  sometimes 
the  row  of  four  is  formed  by  equal  successive  divisions,  it  is 
more  common  for  the  mother-cell  to  elongate  greatly,  with  its 
nucleus  near  the  micropylar  end.  In  this  position  two  succes- 
sive and  rapid  divisions  of  the  nucleus  occur  in  any  order  or 
direction,  and  four  usually  naked  cells  are  the  result,  the  inner- 
most being  much  the  largest  and  speedily  obliterating  the  others^ 
becoming  the  functioning  megaspore  (Fig.  29,  B).  In  Arena 
fatua,  Cannon 86  found  that  four  cells  are  formed ;  or  the 
mother-cell  may  contain  four  nuclei  without  any  cell  walls,  the 
three  outermost  disappearing,  the  innermost  forming  the  nu- 
cleus of  the  functioning  megaspore.  In  Potamogeton  foliosus, 
Wiegand  66  found  that  the  second  divisions  in  forming  the  row 
of  four  are  not  accompanied  by  walls,  and  Holf erty  97  found  in 
Potamogeton  natans  that  the  outermost  wall  may  not  appear 
even  when  there  is  nuclear  division.  Such  cases  emphasize  the 
fact  that  there  may  often  be  the  greatest  variation  in  the  devel- 
opment of  megaspores,  and  that  a  number  reported  for  a  species 
by  a  hasty  observer  should  not  be  regarded  as  a  fixed  one,  or 
even  possibly  the  customary  one. 

The  only  generalization  that  seems  to  be  safe  in  reference 
to  the  Monocotyledons,  aside  from  the  fact  of  their  great  irregu- 
larity, is  that  more  of  them  than  of  the  Dicotyledons  have 
reached  the  condition  of  an  undividing  mother-cell. 

Among  the  Archichlamydeae,  nearly  all  the  species  investi- 
gated have  three  or  four  megaspores,  and  both  of  these  numbers 
are  represented  in  almost  every  family  in  which  more  than  one 
species  has  been  studied.  Upon  the  whole,  however,  a  row  of 
three  megaspores  seems  to  be  more  common  than  one  of  four. 
For  example,  among  the  Ranunculaceae,  of  eleven  genera  stud- 
ied only  four  have  been  reported  as  having  four  megaspores,  and 
in  all  of  these  cases  three  megaspores  have  also  been  observed. 
The  four  genera  referred  to  are  Aquilegia,  in  which  five  mega- 
spores were  also  observed,  Delphinium,  Ranunculus  (Fig.  27), 
and  Thalictrum,  and  in  each  of  these  cases  different  observers 
have  given  different  numbers.  In  Caltha,  which  ordinarily  has 
three  megaspores,  Mottier  36  occasionally  found  nuclear  divi- 


GAMETOPHYTE 

sion,  unaccompanied  by  a  wall,  in  the  outermost  cell  of  the  row 
of  three.  There  is  every  evidence  that  in  this  family  the  inner 
cell  of  the  first  division  always  divides,  and  the  other  one  may 
or  may  not  divide,  resulting  in  three  or  four  megaspores. 
Almost  the  only  exception  to  three  or  four  megaspores,  in  case 
the  mother-cell  divides,  noted  among  Archichlamydeae  is  Vis- 
cniii  articulatum  (Treub13),  in  which  the  four  or  five  mother- 
cells  divide  only  once,  the  inner  cell  becoming  the  functional 
mega  spore./ 

This  same  variation  is  found  in  at  least  twenty  other  fam- 
ilies of  the  Archichlamydeae.  Probably  the  most  variable  case 
recorded  is  that  of  Salix  glaucophylla  (Chamberlain46),  in 
which  there  may  be  three  megaspores,  or  two,  or  the  mother-cell 
may  not  divide. 

The  few  cases  among  Archichlamydeae  in  which  the  mother- 
cells  are  not  known  to  divide  are  three  genera  of  Piperaceae 
(Peperomia,  Piper,  Heckeria)  investigated  by  Johnson,79' 114 
but  the  allied  Saururus  (Johnson87)  has  a  row  of  three  mega- 
spores; Alcliemilla  alpina  (Murbeck94),  but  this  is  associated 
with  the  occurrence  of  a  large  mass  of  archesporial  tissue ;  the 
Cactaceae  (D'Hubert 33) ;  and  at  least  Slum  cicutae  folium 
among  the  Umbelliferae.  In  Juglans  cordiformis  Karsten  115 
finds  great  variability,  the  mother-cell  functioning  directly  as  the 
megaspore  or  giving  rise  to  a  row  of  three  or  four  megaspores, 
the  two  outer  ones  never  functioning,  the  two  inner  ones  appar- 
ently having  an  equal  chance,  and  in  many  cases  developing  two 
sacs.  Among  the  Araliaceae  also,  Ducamp  112  reports  that  the 
mother-cell  becomes  the  megaspore  directly  or  produces  a  row  of 
three  or  four  megaspores.  The  same  is  true  of  the  Balanophora- 
ceae,  as  shown  by  Lotsy  82  in  Rhopalocnemis,  and  by  Chodat 
and  Bernard  83  in  Helosis ;  but  the  conditions  in  this  family  are 
so  peculiar  that  the  phenomenon  does  not  seem  significant.  In 
Casuarina  (Treub25)  (Fig.  24)  and  Quercus  (Conrad78),  in 
which  there  is  a  large  mass  of  sporogenous  cells,  there  is  no 
division  of  mother-cells  to  form  spores.  The  behavior  of  the 
numerous  mother-cells  of  Casuarina  is  remarkable,  a  certain 
number  developing  as  embryo-sacs,  a  larger  number  remaining 
sterile  and  becoming  very  much  elongated,  and  still  others  be- 
coming tracheid-like  cells. 

It  is  apparent,  therefore,  that  among  the  Archichlamydeae 


80  MORPHOLOGY  OF  ANGIOSPERMS 

the  mother-cell  very  rarely  fails  to  divide,  but  that  there  is  a 
strong  tendency  to  suppress  one  of  the  divisions  and  form  a 
row  of  three  megaspores. 

Among  the  Sympetalae  the  complete  tetrad  appears  with 
remarkable  uniformity.  This  is  associated  with  a  very  small 
nucellus,  most  frequently  only  the  epidermal  layer  investing 
the  tetrad  row,  and  the  suggestion  is  evident  that  there  may  be 
some  causal  relation  between  these  two  facts.  Occasionally, 
however,  one  of  the  divisions  is  suppressed,  and  a  row  of 
three  megaspores  is  the  result,  the  only  cases  we  have  found 
being  Vaccinium  and  Lycium  (Vesque4),  Lobelia  (Marshall- 
Ward8),  Lonicera  and  Nicotiana  (Guignard  12),  and  Trapella 
and  Sarcodes  (Oliver21'  24).  Among  the  Rubiaceae  Lloyd105 
reports  that  while  each  mother-cell  forms  a  tetrad  there  are 
usually  no  walls  (Fig.  33),  as  in  Avena  (Cannon86)  and  Eich- 
hornia  (Smith53).  Among  the  Verbenaceae  Treub  14  reports 
that  in  Avicennia  officinalis  the  mother-cell  does  not  divide ;  in 
Aphyllon  uniflorum  Miss  Smith  102  reports  that'  the  mother- 
cell  does  not  divide,  although  Koch 19  figures  a  row  of  four 
megaspores  in  Orobanche ;  in  the  parthenogenetic  Antennaria 
alpina  Juel  74  finds  that  the  mother-cell  does  not  divide,  how- 
ever, in  A.  dioica,  in  which  fertilization  regularly  occurs,  a 
row  of  four  megaspores  is  formed.  Undoubtedly  more  numer- 
ous exceptions  will  be  found,  but  the  evidence  seems  clear  that 
the  complete  row  of  four  megaspores  is  almost  universally  pres- 
ent among  the  Sympetalae. 

As  has  been  stated,  the  reduction  in  the  number  of  chromo- 
somes occurs  during  the  first  mitosis  in  the  megaspore-mother- 
cell,  whether  a  row  of  four,  or  three,  or  two  megaspores  is  to 
be  formed,  or  the  mother-cell  is  to  function  directly  as  a  mega- 
spore.  In  Lilium,  the  first  described  form  in  which  the  mother- 
cell  does  not  divide  to  form  megaspores,  the  beginning  of  a 
cell-plate  is  clearly  visible  in  the  spindle  during  the  first  mito- 
sis, and  at  the  second  mitosis  there  is  also  a  rudimentary  cell- 
plate.  Since  the  other  cytological  characters  of  these  two  mito- 
ses are  identical  with  the  first  two  mitoses  in  forms  that  have' 
the  row  of  four  megaspores,  it  might  be  suggested  that  the 
rudimentary  plate  is  a  survival,  indicating  that  the  ancestors 
of  Lilium  once  produced  the  row  of  four,  and  making  Lilium 
in  this  respect  a  specialized  rather  than  a  primitive  form.  This 


THE  FEMALE  GAMETOPHYTE 


81 


seems  reasonable,  but  it  must  be  noted  that  the  rudimentary 
plate  occurs  also  at  the  third  mitosis,  and  so  may  be  a  reminis- 
mce  of  a  much  more  remote  ancestry  with  cellular  prothallia. 
In  connection  with  the  reduction  division  it  is  of  interest 
to  note  the  number  of  chromosomes  found  among  Angiosperms. 
The  following  table,  arranged  in  the  Engler  sequence  of  fami- 
lies, although  more  extensive  than  any  hitherto  published,  is 
far  from  complete.  The  numbers  in  parentheses  were  inferred 
rather  than  actually  counted: 

Th  e  Number  of  Chromosomes  recorded  for  Certain  Angiosperms 


PLANT. 

CHROMOSOME   NUMBERS. 

Observer. 

Year. 

Gameto- 
phyte. 

Sporophyte. 

Zostera  marina  

6 
6 
8 
8 
12 
16 
8 
12* 
24 
8 
8 
(8) 
12 
12 
12 
12 
12 
12 
12 
12 
12 
8 
12 
8 
8 
8 
24 
16? 
18 
<> 
6 
12 
8 
8 
12 
3 
16 

12 

12 
(16) 
16 
mostly  16 
(32) 
16 
t 
(48) 
16 
(16) 
16 
mostly  16 

24 
24 

24 
24 
24 
24 
24 
16 
24 
16  or  less 
(16) 
'variably  8-16 
48 
more  than  16 
(36) 
12 
12 
(24) 
mostly  16 
16 
24 
6 
32 

Rosenberg92 
Guignard  n 
Overton  28 
Koernicke  ** 
Strasburger20 

Smith53 
« 

Strasburger  ™ 
Strasburger  72 
Strasburger  20 
Guignard  26 
Schaffner  55 
Strasburger  20 
Guignard  16 
Sargant  41 
Strasburger  20 

Schaffner48 

Strasburger  20 
Guignard  26 
Schn.-Thies95 
Schaffner98 
Schn.-Thies95 
Overton  28 
Schn.  -Thies  95 
Strasburger  20 

Wiegand  M 
Atkinson  w 
The  authors. 
Overton  28 
Strasburger  20 
Guignard26 
Strasburger  « 
Wiegand80 
Strasburger  M 

1901 
1899 
1893 
1896 
1888 
1898 
1898 
1888 
1900 
1888 
1891 
1898 
1888 
1884 
1896 
1888 
1888 
1897 
1897 
1888 
1891 
1901 
1901 
1901 
1893 
1901 
1888 
1888 
1900 
1899 
1902 
1893 
1888 
1891 
1900 
1900 
1888 

Rains  major 

Triticum  vulgare 

Tradescantia  

EicHhomia  crassipes  

Pontederia  cordata  t.  .  . 

ChloropJiytum  Sternbergianum  . 
FH  nkia  Sieboldiana 

AUiutn  fistulosum  

ursinum  

'  '       Cepa  

lAHum 

'       Mart  agon 

'       candidum  

croccnm  

ph  i  ladnlphiciim 

'       tigrinum 

Fritilliirici  imperialis 

Meleagris  
Tulipa  Gesneriana  

Erythronium  americanum  
Graltonia  candicans  

Scilla  non-scripfa 

"      sibirica      

JKfMgeor*  ncglectum  

Conrallaria  majalis  

Trillium  grandiflorum 

"         recurvatum  

Lmcojum  vernum  

Alstroemeria 

psitfacea  .    . 

J/-/x  xqualens  

Can  n  a  tndica  

Cypripedium  barbatnm.  . 

*  One  anther  constantly  14. 


82 


MORPHOLOGY  OF  ANGIOSPERMS 


The  Number  of  Chromosomes — Continued 


PLANT. 

CHROMOSOME  NUMBERS. 

Observer. 

Year. 

Gameto- 
phyte. 

Sporophyte. 

Orchis  mascula 

16 
16 
16 
16 
16 
32 
48 
12 
12 
12 
12 
12 
8 
32 
10 
10 
12 
10 
40-50 
12-14 
8 
8 

(32) 
(32) 
(32) 
(32) 
(32) 
(64) 
(96) 
24 
(24) 
24 
mostly  16 
(24) 
16 
32 
20 
20 
24 
20 
40-50 
counted  20 
(16) 
16f 

Strasburger  20 

Guignard  26 

Guignard  59 
Strasburger  72 
Strasburger  108 
Overton  28 
Strasburger  20 
Strasburger  30 
Overton  28 
Mottier34 
Murbeck  94 
Strasburger  % 
Frye  " 
Lloyd105 

Juel88 

Merrell  77 
Land  81 

1888 
1888 
1888 
1891 
1891 
1898 
1900 
1902 
1893 
1888 
1894 
1893 
1895 
1901 
1901 
1901 
1902 
1902 
1900 
1900 
1900 
1900 

Himantoglossum  hircinum  
Gymnadenia  conopsea  

Listera  ovata  

Neottia  nidus-avis 

Nymphaea  alba, 

Ceratophyllum  submersum  

Aconitum  Napellus 

Helleborus  foelidus 

Paeonia  spectabilis    

Podophyllum  pcltatum 

Alchemilla  alpina  * 

Asclf-pias  Cornuti 

"        tuberosa      

Asperula  

Crucianella  

Antennaria  alpina*  

'  '           dioica 

Silphium  inteqrifolium 

'  '        laciniatum  

It  is  evident  from  the  table  that  Strasburger  and  Guignard 
were  pioneers  in  this  work  and  that  they  still  remain  the  most 
active  contributors.  It  is  of  interest  to  note  that  when  atten- 
tion was  first  directed  to  this  subject,  the  number  of  chromo- 
somes reported  for  the  sporophyte,  while  exceeding  that  of  the 
gametophyte,  was  not  precisely  twice  that  number.  The  sub- 
ject is  one  of  great  difficulty,  and  doubtless  the  countings  of 
competent  investigators  have  often  been  influenced  by  their 
theories,  while  their  followers  have  been  content  too  often  with 
confirming  a  reported  number.  Variations  from  the  character- 
istic number  are  numerous.  In  the  gametophyte  the  number 
of  chromosomes  in  the  antipodals  is  frequently  irregular,  with 
a  tendency  to  higher  numbers ;  but  an  explanation  may  be  found 
in  the  irregular  nuclear  divisions  which  present  some  of  the 
characters  of  amitosis  (Miss  Sargant41).  Variations  are  even 
more  frequent  in  the  sporophyte,  but  it  is  well  known  that 
mitoses  are  frequently  irregular,  and  it  is  easy  to  imagine  that 
a  chromosome  may  fail  to  split  or  that  an  unequal  distribu- 


*  Parthenogenetic. 


f  More  than  16,  probably  24,  in  endosperm. 


THE  FEMALE  GAMETOPHYTE  83 

tion  to  the  daughter  nuclei  may  occur.  The  high  numbers 
reported  for  the  endosperm  are  doubtless  to  be  explained  by 
the  triple  fusion. 

In  the  great  majority  of  cases  the  gametophyte  number  has 
been  counted  only  in  the  mother-cells,  and  the  sporophyte  num- 
ber in  the  tissues  of  the  ovule  or  young  embryo.  Still,  occa- 
ional  counts  throughout  the  entire  life-history  show  that  the 
reduced  number  that  occurs  in  the  division  of  the  mother-cell 
is  maintained  up  to  the  time  of  fertilization,  whether  the  inter- 
val be  short,  as  in  Angiosperms,  where  only  from  three  to  five 
nuclear  divisions  intervene  between  reduction  and  fertiliza- 
tion, or  long,  as  in  the  liverworts,  where  the  gametophyte  is  the 
more  permanent  generation  and  the  sporophyte  is  a  compara- 
tively temporary  structure. 

Why  the  number  of  chromosomes  should  be  so  constant,  and 
why  a  reduction  in  number  should  take  place,  are  the  most 
important  questions  in  this  connection.  The  constancy  of  the 
numbers  has  led  many  to  believe  that  the  chromosome  is  a 
permanent  organ  of  the  nucleus,  just  as  the  latter  is  a  perma- 
nent organ  of  the  cell ;  but  no  one  would  assign  such  a  reason 
for  the  constant  recurrence  of  six  stamens  in  a  lily.  There  is 
other  evidence  in  favor  of  the  individuality  of  the  chromosomes, 
but  it  does  not  seem  to  be  .sufficient.  The  physiological  advan- 
tages are  evident,  for  the  constancy  in  number  enables  each 
parent  to  transmit  an  equal  number  of  chromosomes  to  the  off- 
spring, and  the  reduction  prevents  the  constant  geometrical 
increase  in  the  number  of  chromosomes  which  would  otherwise 
occur.  Strasburger  108  says :  "  The  morphological  cause  of  the 
reduction  in  the  number  of  the  chromosomes  and  of  their  equal- 
ity in  number  in  the  sexual  cells  is,  in  my  opinion,  phylogenetic. 
I  look  upon  these  facts  as  indicating  a  return  to  the  original 
generation  from  which,  after  it  had  attained  sexual  differentia- 
tion, offspring  were  developed  having  the  double  number  of 
chromosomes.  Thus  the  reduction  by  one-half  of  the  number 
of  chromosomes  in  the  sexual  cells  is  not  the  outcome  of  a 
gradually  evolved  process  of  reduction,  but  rather  it  is  the  reap- 
pearance of  the  primitive  number  of  chromosomes  as  it  existed 
in  the  nuclei  of  the  generation  in  which  sexual  differentiation 
first  took  place.  .  .  .  The  reduction  in  the  number  of  chromo- 
somes takes  place,  in  the  higher  plants,  in  the  mother-cells  of 


84  MORPHOLOGY  OF  ANGIOSPERMS 

the  spores,  and  it  is  consequently  these  which  must  be  regarded 
as  the  first  term  of  the  new  generation." 

In  case  the  mother-cell  divides,  only  the  innermost  mega- 
spore  functions,  its  growth  involving  the  digestion  and  absorp- 
tion of  the  other  megaspores,  as  well  as  more  or  less  of  the  sur- 
rounding sterile  tissue.  Ordinarily  the  elongating  megaspore 
encroaches  upon  the  others  until  they  become  merely  a  cap  upon 
it;  but  among  the  Ranunculaceae  Guignard  12  found  in  Cle- 
matis and  Helleborus,  and  Mottier  3G  in  Delphinium,  that  the 
nucellus  elongates  so  rapidly  that  the  sterile  megaspores  are 
not  crowded  into  a  cap,  but  their  disorganization  leaves  a  nar- 
row cavity.  The  same  thing  occurs  in  Jeffersonia,  as  shown 
by  Andrews,37  and  doubtless  among  many  other  Archichla- 
mydeae.  The  known  exceptions  to  the  functioning  of  the  inner- 
most megaspore  are  so  few  that  they  deserve  special  mention, 
as  possibly  indicating  some  peculiar  condition. 

Among  the  Monocotyledons,  Agraphis  (S cilia)  and  Dieffen- 
bachia  are  the  only  exceptions  we  have  noted.  In  the  former, 
Treub  and  Mellink  10  observed  that  the  outer  one  of  the  two 
megaspores  becomes  the  embryo-sac,  but  the  inner  one  also  de- 
velops a  sac  to  the  four-nucleate  stage,  an  observation  later  con- 
firmed by  Guignard  12  for  other  species  of  the  genus.  In  Agra- 
phis  nulans  Vesque  4  observed  the  uppermost  of  a  row  of  three 
megaspores  functioning,  but  the  ordinary  divisions  within  the 
embryo-sac,  up  to  four  nuclei,  were  also  observed  in  two  or 
even  all  of  the  megaspores.  The  same  observer  also  reports 
that  in  Yucca  gloriosa  all  four  megaspores  show  sac  tendencies, 
while  in  Uvularia  each  spore  in  a  row  of  two  developed  an 
embryo-sac  to  the  four-nucleate  condition.  In  Dieffenbachia, 
Campbell  75  says  that  the  mother-cell  divides  very  unequally, 
the  outer  one  being  the  larger  and  developing  the  embryo-sac. 
In  Galtonia  candicans  (Liliaceae)  Schniewind-Thies  95  has  ob- 
served an  interesting  transition  4o  the  condition  of  Lilium  and 
similar  forms.  The  mother-cell  usually  gives  rise  to  a  row  of 
four  megaspores,  but  occasionally  only  two  spores  appear,  one 
of  which  may  pass  over  directly  into  the  embryo-sac. 

Among  the  Archichlamydeae,  in  Juglans  cordiformis  (Kar- 
sten115),  the  two  chalazal  megaspores  may  both  develop  em- 
bryo-sacs; the  outermost  megaspore  of  the  row  often  functions 
in  Stellaria  Holostea  (Vesque4)  and  in  Rosa,  and  sometimes 


THE  FEMALE  GAMETOPHYTE 


in  the  latter  the  two  outer  begin  the  formation  of  embryo-sacs ; 
and  in  Eriobotrya  Guignard  12  found  that  while  ordinarily  the 
innermost  megaspore  of  three  functions,  the  middle  or  the  outer 
one  may  form  the  embryo-sac,  and  even  all  three  may  begin  its 
formation.  The  same  author11  also  reports  great  irregularity 
in  Acacia,  in  some  species  the  innermost  of  four  megaspores 
functioning,  in  others  the  next  outer  one,  and  in  still  others 
the  middle  one  of  a  row  of  three.  In 
Lorantlius  also,  Treub  13  finds  that  the 
outermost  megaspore  of  three  persist- 
ently functions.  Among  the  Aralia- 
ceae  (Ducamp112)  usually  the  inner- 
most of  four  megaspores  functions,  but 
occasionally  one  of  the  middle  cells 
may  become  the  embryo-sac.  Such 
cases  serve  to  emphasize  the  megaspore 
character  of  all  the  cells  of  the  row. 

Among  the  Sympetalae,  the  only 
well-established  exception  is  that  of 
TrapeUa,  in  which  Oliver  21  finds  that 
the  outermost  of  four  megaspores  func- 
tions, and  in  one  case  the  next  cell, 
while  the  innermost  megaspore  devel- 
ops the  remarkable  haustorium  (Fig. 
32).  In  Asdepias  iuberosa,  although 
the  innermost  of  the  row  of  four  mega- 
spores ordinarily  functions,  Frye 118 
has  observed  cases  in  which  the  outer- 
most megaspore  functions,  and  others 
in  which  the  two  innermost  develop 
together ;  while  Vesque  4  reports  that 
in  Sal  via  praiensis  the  outermost  of 
the  four  megaspores  functions.  In  Crucianella  (Lloyd 105) 
all  four  megaspores,  which  in  this  case  are  not  separated  by 
cell-walls,  may  begin  to  germinate  (Fig.  33).  Guignard12 
also  includes  Pyreihrwn  as  among  the  forms  whose  outer- 
most megaspore  functions,  but  it  needs  further  investigation. 
It  should  be  noted  in  this  connection  that  when  a  row  of  four 
megaspores  is  to  be  formed,  the  nucleus  nearest  the  chalaza  al- 
most invariably  shows  a  more  advanced  stage  in  mitosis  than 


FIG.  32.  —  Trajjdla  sinensi*. 
Ovule  some  time  after  fer- 
tilization: m,  micropyle;  *, 
synergids ;  «p,  suspensor ;  ^, 
embryo;  e,  endosperm;  «, 
vascular  bundle ;  c,  two  long 
cells  resulting  from  the  lon- 
gitudinal division  of  the  low- 
ermost megaspore  of  a  row 
of  four;  x  100.— After  OLI- 
VER.*1 


86 


MORPHOLOGY   OF  AXGIOSPERMS 


the  nucleus  nearer  the  micropyle,  as  shown  far  Trillium  in 
Fig.  28.  Hence  the  megaspore  at  the  chalazal  end  of  a  row 
is  formed  a  little  earlier  than  the  one  at  the  micropylar  end. 


V 


A  B  C 

FIG.  33. —  Crucianella  macrostachya.  A,  four-nucleate  embryo-sac  and  three  disintegra- 
ting megaspores  ;  the  four  megaspores  of  this  axial  row  not  separated  by  cell-walls. 
B,  axial  row  of  four  megaspores  which  are  not  separated  by  cell-walls ;  each  mega- 
spore  has  germinated  and  is  in  the  binucleate  stage.  (7,  an  embryo-sac  (with  two 
nuclei)  and  four  sets  of  megaspores ;  the  megaspores  of  one  set  germinating. — After 

LLOYD.106 

A  still  more  important  reason  for  the  selection  of  the  chalazal 
megaspore  is  doubtless  its  more  immediate  relation  to  the  nutri- 
tive supplies  coming  through  the  base  of  the  ovule,  a  fact  which 
may  also  account  for  the  earlier  mitosis  at  the  chalazal  end  of 
the  row. 

In  case  there  is  more  than  one  mother-cell,  two  or  more 
megaspores  may  begin  the  development  of  embryo-sacs,  which 
may  even  attain  the  fertilization  stage,  but  in  almost  every  case 
one  embryo-sac  prevails  over  the  others.  Among  the  Monocoty- 
ledons two  embryo-sacs  are  reported  as  sometimes  occurring  in 
Lilium  candidum  (Bernard 84) ;  and  in  Agraphis  (Vesque,4 
Guignard  12)  and  Uvularia  (Vesque4),  as  referred  to  above, 
all  of  the  two  or  three  megaspores  of  the  single  row  develop 
embryo-sacs  to  the  four-nucleate  stage.  Among  the  Archichla- 
mydeae,  five  to  eight  sacs  begin  to  develop  in  Loranthus 


THE   FEMALE   GAMETOPHYTE 


87 


(Treub15)  and  in  Casuarina  (Treub  25)  ;  in  Viscum  articula- 
tum  (Treub13)  all  of  the  four  or  five  megaspores  reach  the 
two-nucleate  stage;  in  Salix  (Chamberlain46)  occasionally  two 
embryo-sacs  are  found  in  the  fertilization  stage;  in  Fagus, 
Corylus,  and  Carpinus  (Miss  Benson  31)  two  or  more  completed 
sacs  have  been  observed;  in  Juglans  cordiformis  (Karsten115) 
two  embryo-sacs  often  occur;  in  Delphinium  (lEottier36)  two 
completed  embryo-sacs  have  been  found  (Fig.  34),  and  in  Ra- 
nunculus (Coulter51)  several  sacs  develop  to  the  two  or  four- 
nucleate  stage  (Fig.  25)  ;  among  the  Kosaceae,  several  embryo- 
sacs  have  been  observed  to  start  in  Rosa  (Strasburger  5),  Erio- 
botrya  (Guignard  12),  and  AlchemiUa  (Murbeck94);  and  the 
same  is  true  of  Astilbe  (Webb111).  Among  the  Compositae, 
Marshall-Ward  8  observed  three  sacs  enlarging  side  by  side  in 
Pyrethrum,  and  Mottier29  reports  two  completed  sacs  in 
Senecio. 

The  history  of  the  gametophyte  from  the  megaspore  to  the 
completion  of  the  egg-apparatus  is  remarkably  uniform.  Atten- 
tion has  been  focused  upon  it  for 
many  years,  and  almost  every 
description  is  a  reiteration  of 
the  preceding  one.  The  mega- 
spore  and  its  nucleus  usually  en- 
large very  much  before  division, 
and  the  daughter  nuclei  migrate, 
one  to  each  end  of  the  sac  (Figs. 
35-37).  The  subsequent  divi- 
sions proceed  rapidly  and  simul- 
taneously, resulting  in  a  group 
of  four  nuclei  at  each  end  of  the 
embryo-sac.  The  antipodal  po- 
lar nucleus  and  the  micropylar 
polar  nucleus  (sister  to  the  egg) 

then  move  toward  one  another  and  fuse  in  the  general  central  re- 
gion of  the  sac,  forming  the  primary  endosperm  nucleus.*  The 
three  remaining  micropylar  nuclei  enter  into  the  formation  of 
the  cells  of  the  egg-apparatus,  while  the  three  remaining  antipo- 
dal nuclei  enter  into  the  formation  of  the  antipodal  cells.  Such 

*  A  discussion  of  the  participation  of  one  of  the  male  cells  in  the  forma- 
tion of  this  nucleus  will  be  found  in  Chapter  VII. 

7 


FIG.  34.— Delphinium  tricorne.  Two  ma- 
ture embryo-sac?  lying  side  by  side  in 
one  ovule  :  x  250.— After  MOTTIER." 


88 


MORPHOLOGY  OF  ANGIOSPERMS 


is  in  brief  outline  a  history  whose  beginnings  are  entirely  con- 
jectural. Its  uniformity  throughout  so  vast  a  group  of  plants 
testifies  to  its  long  establishment.  The  evanescent  cell-plate 
frequently  observed  during  the  three  free  nuclear  divisions  by 


FIG.  37. — -4,  Lilium  philadelphicum,  second  nuclear  division  in  the  embryo-sac ;  the 
persistence  of  the  spindle  from  the  first  division  indicates  that  the  second  division 
has  followed  very  rapidly;  x  450;  after  ScnAFFNER.48  B,  L.  pJiiladelphicitm, 
third  nuclear  division ;  two  of  the  spindles  show  the  beginning  of  a  cell-plate ; 
x  450 ;  after  COULTER."  C",  Ranunculus  multifidus,  fusion  of  polar  nuclei  to  form 
endosperm  nucleus;  x  600;  after  COULTER « ;  *,  synergids;  o,  oosphere,  fusing 
polar  nuclei  in  central  region :  a,  antipodals. 

which  the  eight-nucleate  stage  of  the  embryo-sac  is  reached,  the 
frequent  organization  of  cells  about  the  three  antipodal  nuclei, 
the  frequent  division  of  the  antipodal  cells  resulting  in  a  more 
or  less  extensive  tissue,  and  the  additional  nuclear  divisions  ob- 
served in  Peperomia  and  other  forms,  are  evidences  that  the 
present  female  gametophyte  of  Angiosperms  is  a  much  reduced 
descendant  from  multicellular  ancestral  forms,  with  forms  like 
Gnetum  as  the  nearest  approach  to  the  present  conditions;  but 
there  seem  to  be  no  nearer  records  of  its  connection  with  the 
histories  of  other  female  gametophytes.  The  female  gameto- 
phyte of  Angiosperms,  therefore,  is  a  morphological  problem  of 


. 


FIG.  35. — Lilitim  pkttaeUXph&cwn.  A,  archesporial  cell  which  is  also  the  megaspore 
mother-cell ;  £.  synapsis  ;  C.  stage  just  before  splitting  of  spirem :  D,  longitudinal 
splitting  of  spirem  (best  seen  in  threads  at  the  left) ;  x  466. — Negatives  by  W.  J. 
G.  LAND. 


G  H 

FIG.  36. — Lilium  ptiiladelphicum.  E,  mitotic  figure  of  the  reduction  division  showing- 
the  short,  thick  chromosomes  characteri'stic  of  this  stage ;  F,  binucleate  embryo- 
sac  ;  G,  four-nucleate  embryo-sac  ;  H, "  double  fertilization  " ;  in  the  egg  the  darker 
nucleus  is  the  male  and  the  lighter  one  the  female;  just  beyond  the  egg  three 
nuclei  are  fusing;  the  antipodal  polar  nucleus  forms  about  one-half  of  the  complex, 
while  the  micropylar  polar  nucleus  and  the  male  nucleus  form  the  other  half,  the 
male  nucleus  being  on  the  right  and  touching  both  polar  nuclei.  E-G  x  466;. 
H  x  520.— Negatives  by  W.  J.  G.  LAND. 


THE  FEMALE  GAMETOPHYTE 


89 


great  obscurity,  and  very  little  has  been  added  to  the  original      ._ 
suggestions  concerning  it. 

The  most  important  departure  from  the  ordinary  history 
is  that  shown  by  Peperomia  pelhicida,  as  described  by  Camp- 
bell 70  and  Johnson79  (Fig.  38),  Gunnera  (Schnegg103),  Tril- 
lium (Ernst116),  and  Tulipa  as  described  by  Guignard.89*  In 
Peperomia  the  nuclei  of  the  embryo-sac  do  not  show  any  of  the 
polarity  that  is  so  marked  a  feature  in  other  forms.  The  first 
four  nuclei  are  large,  and  arranged  peripherally  like  the  spores 
of  a  tetrad.  Divisions  continue  until  sixteen  parietal  nuclei, 
rather  evenly  distributed,  are  found  in  the  sac.  One  of  the 
nuclei  at  the  micropylar  end  of  the  sac  becomes  somewhat  larger 
and  is  surrounded  by  a  fairly  defined  mass  of  cytoplasm  with  a 
limiting  membrane,  this  cell  functioning  as  the  egg.  Another 
micropylar  cell  is  similarly  organized,  and  from  its  position 


A 


D 


FIG.  3S. — Peperomia  pellucida.  A,  longitudinal  section  of  an  ovule  with  a  four-nucleate 
embryo-sac  showing  no  polarity  ;  x  295.  B,  embryo-sac  at  time  of  fertilization ;  tt 
pollen-tube;"o,  oospore;  <-,  group  of  nuclei  fusing  to  form  endosperm  nucleus  ;jt>, 
peripheral  nucleus  of  embryo-sac ;  £,  synergid ;  v,  vacuole ;  x  520.  C,  Z),  groups  of 
nuclei  fusing  to  form  endosperm  nucleus ;  x  520. — After  JOHNSON.™ 

may  be  called  a  synergid.  Eight  of  the  remaining  nuclei  mass 
together,  are  surrounded  by  a  common  cytoplasmic  investment, 
and  after  fertilization  unite  to  form  a  great  fusion-nucleus  that 
functions  as  the  primary  endosperm  nucleus.  The  remaining 
six  nuclei  remain  in  their  parietal  position  and  are  finally  cut 


90 


MORPHOLOGY  OF  ANGIOSPERMS 


off  by  walls,  showing  no  tendency  to  migrate  toward  the  posi- 
tion of  antipodal  cells.     This  remarkable  history  is  regarded  by 

Campbell  as  repre- 
senting a  primitive 
phase  of  the  embryo- 
sac  of  Angiosperms ; 
a  view  from  which 
Johnson  dissents,  and 
in  a  more  recent  pa- 
per 114  he  shows  that 
in  the  allied  Piper 
and  Heckeria  the 
eight-nucleate  stage 
of  the  embryo-sac  is 
reached  in  the  usual 
way.  It  is  tempting 
to  connect  such  a  sac 
as  that  of  Peperomia 
with  such  as  that  of 
Gnetum,  and  theo- 


FIG. 39. —  Gunnera.  A,  embryo-sac  with  nine  nuclei, 
showing  no  polarity.  B,  later  stage  showing  sixteen 
nuclei ;  «,  synergid  nuclei ;  0,  oosphere  nucleus ;  near 
center,  a  group  of  six  nuclei  fusing  to  form  endosperm 
nucleus;  near  base,  seven  antipodal  nuclei. — After 

SCHNEGG.108 


retically  it  repre- 
sents what  one  might  expect  to  be  an  earlier  condition  of 
the  female  gametophyte  among  Angiosperms;  but  Johnson  in- 
fers from  the  testimony  of  Piper  and  Heckeria,  just  referred 
to,  that  this  particular  sac  of  Peperomia  is  specialized  rather 
than  primitive. 

In  Gunnera,  according  to  Schnegg,103  there  is  no  polarity 
in  the  early  stages  of  the  embryo-sac,  and  the  nuclear  divisions 
are  not  simultaneous  but  irregular,  so  that  there  is  no  definite 
eight-nucleate  stage  of  the  sac.  Before  fertilization  there  are 
"  at  least  "  eight  nuclei,  and  very  commonly  one  or  more  of  the 
nuclei  divide  so  that  nine  or  ten  and  sometimes  even  sixteen 
nuclei  are  found  (Fig.  39)  ;  in  which  case,  as  in  Peperomia, 
the  primary  endosperm  nucleus  is  formed  by  the  fusion  of  a 
considerable  number  of  nuclei.  A  similar  lack  of  polarity  has 
been  observed  in  Tulipa  sylvestris  by  Gnignard,890  and  in  Tril- 
lium grandiflorum  by  Ernst116;  in  the  latter  case  at  least  two 
of  the  nuclei  of  the  eight-nucleate  sac  have  been  known  to  di- 
vide, giving  rise  to  a  sac  with  ten  nuclei. 

In  the  embryo-sac  of  Juglans  regia  Xawaschin  38  has  indi- 


THE  FEMALE  GAMETOPHYTE 


91 


cated  a  lack  of  the  usual  definite  organization,  the  male  cells 
being  described  as  "  wandering  "  in  the  cytoplasm  of  the  sac 
and  fusing  with  one  of  several  free  nuclei  which  function  as 
eggs  but  have  not  organized  into  an  egg-apparatus.  This  loose- 
ness of  organization  in  the  cells  of  the  embryo-sac  has  also  been 
observed  by  Karsten115  in  several  species  of  Juglans,  and  he 
emphasizes  the  resemblance  to  Gymnosperms,  believing  that 
Angiosperms  are  derived  from  them,  with  such  forms  as 
One  turn  as  the  point  of  origin. 

What  may  be  called  minor  irregularities  in  the  structure  of 
the  female  gametophyte  have  been  described  in  a  number  of 
forms.  The  reported  occurrence  of  only  one  synergid  in  Ornir 


w-  c 


B 


FIG.  40. — Helosis  guyanensis.  A,  binucleate  embryo-sac  with  antipodal  nucleus  already 
disintegrating.  £,  later  stage  ;  micropylar  nucleus  has  divided  twice,  giving  rise  to 
two  synergids,  an  egg  (not  shown),  and  the  micropylar  polar  nucleus  which  gives 
rise  to  the  endosperm;  no  antipodals.  (7,  remains  of  synergids  and  egg;  the 
"pseudo-endosperm"  nucleus  dividing;  no  trace  of  antipodals. — After  CHODAT  and 

BERNARD.83 

ihogalum  nutans,  Santalum,  Gomphrena,  and  LorantTius,  has 
long  been  known.  In  Loranthus  Treub  13  says  that  this  is  due 
to  the  fact  that  the  primary  micropylar  nucleus  divides  only 
once,  but  it  is  also  possible  that  the  mother-nucleus  of  the 


92 


MORPHOLOGY  OF  ANGIOSPERMS 


synergids  may  not  always  divide.  In  the  same  category  Casu- 
arina,  as  reported  by  Treub,25  has  long  been  included;  but  a 
recent  study  of  the  genus  by  Frye  119  has  shown  that  the  usual 
three  micropylar  nuclei  occur.  Fischer  6 
reports  the  occurrence  of  two  eggs  in 
Gomphrena,  which  Strasburger  suggests 
may  have  come  from  division  of  the  nor- 
mal egg. 

In  Loranthus  and  Casuarina  Treub 
also  states  that  there  are  no  antipodals; 
but  Frye's  119  recent  investigation  of  the 
latter  form  has  resulted  in  the  discovery 
of  three  antipodals,  which  occur  either 
at  the  chalazal  extremity  of  the  expand- 
ed portion  of  the  sac,  or  in  the  tubular 
haustorial  elongation. 

In  Helosis  guayanensis  (Balanopho- 
raceae)  Chodat  and  Bernard  83  state  that 
the  primary  antipodal  nucleus  (binu- 
cleate  stage)  rarely  divides,  but  soon  de- 
generates, which  means  also  the  absence 
of  an  antipodal  polar  nucleus  (Fig.  40). 
The  same  phenomenon  has  been  ob- 
served by  Hall109  in  Limnocharis,  the 
primary  antipodal  nucleus  remaining 
undivided.  Several  cases  have  also  been 
reported  in  which  regularly  formed  po- 
lar nuclei  approach  one  another  but  do 
not  fuse  before  endosperm  formation,  as 
in  Balanophora  elongata  (Treub32), 
confirmed  also  in  B.  indica  by  Van  Tie- 
ghem,45  and  in  B.  globosa  by  Lotsy  69 ; 
but  in  the  allied  Rhopalocnemis  (Lot- 


Fio.  41. — Antennaria  alpina. 
Egg-cell  much  extended 
and  polar  nuclei  about  to 
divide ;  a,  antipodal  cells ; 
ei  e£g  >  Pi  polar  nuclei ;  *, 
synergid;  m,  micropyle; 
x  250.— After  JUEL.™ 


sy82)  the  polar  nuclei  fuse.  In  the  or- 
chid Gymnadenia  also,  Marshall-Ward  7 
states  that  the  polar  nuclei  do  not  fuse; 

in  the  parthenogenetic  Antennaria  alpina  Juel  57  (Fig.  41)  ob- 
served the  same  phenomenon ;  in  Lemna  Caldwell  62  reports  that 
the  polar  nuclei  often  do  not  fuse ;  and  in  Juglans  nigra  Kar- 
sten  115  states  that  there  is  probably  no  fusion  of  polar  nuclei,  or 


THE  FEMALE  GAMETOPHYTE 


93 


if  it  takes  place  at  all  it  is  very  late.  In  parthenogenetic  species 
of  Alcliemilla  (Murbeck  11S),  not  only  the  two  polar  nuclei  have 
the  power  of  motion,  but  the  synergid  and  antipodal  nuclei  may 
also  move  toward  the  center  of  the  sac,  forming  groups  of  three, 
four,  or  five  "  polar  nuclei "  surrounded  by  a  common  mass  of 
protoplasm.  In  the  case  represented  in  Fig.  42,  Murbeck  inter- 
prets the  antipodals  to  be  lacking,  although,  according  to  his 
own  account,  their  nuclei  are  in  the  group 
of  what  he  calls  "  polar  nuclei." 

Xotwithstanding  some  such  irregulari- 
,  ties,   however,   the  normal  history  of  the 
female  gametophyte  is  so  remarkably  con- 
stant that  none  of  them  can  be  regarded 
as  of  special  significance. 

The  cells  of  the  egg-apparatus  are  alike 
in  being  pyriform  and  bounded  by  a  mem- 
brane which,  for  the  lack  of  an  accepted 
English  equivalent,  is  commonly  desig- 
nated the  Hautschicht;  the  egg,  however, 
is  vacuolate  toward  the  micropyle,  its  nu- 
cleus lying  at  its  broad  extremity,  while  in 
the  synergids  the  reverse  is  true  (Fig.  43). 
The  size  of  these  cells,  as  compared  with 
the  other  cells  of  the  embryo-sac,  is  ex- 
ceedingly variable,  sometimes  being  much 
the  largest  and  sometimes  even  the  small- 
est. The  morphological  nature  of  this 
group  of  cells  has  been  much  discussed  in 
the  attempt  to  relate  it  to  the  archegonium 
-of  the  lower  plants.  There  seems  to  be  no 
serious  objection  to  regarding  all  three 
cells  as  potential  eggs,  only  one  of  which 
usually  functions  as  such.  Whether  they 
represent  three  archegonia,  or  the  egg  and  canal  cells  of  one 
archegonium,  seems  to  be  pressing  morphology  to  an  absurdity. 
The  lack  of  any  compact  tissue  precludes  the  formation  of  an 
archegonium,  and  hence  free  cells  organize  as  eggs.  There 
seems  to  be  no  need  to  relate  them  to  archegonia,  but  merely 
regard  them  as  eggs  produced  by  a  gametophyte  that  can  not 
form  archegonia.  If  a  rigid  morphology  is  to  be  applied,  it 


FIG.  4.2—Alchemilla  sert- 
cata.  "  Embryo-sac  with 
complete  egg-apparatus 
and  five  polar  nuclei ;  in 
agreement  with  this,  no 
antipodals  are  present" 
—After  MUBBECK.I" 


94 


MORPHOLOGY  OF  ANGIOSPERMS 


may  be  said  that  these  eggs  appear  earlier  in  the  history  of  the 
gametophyte  than  is  possible  for  archegonia,  which  are  rela- 
tively late  structures. 

The  character  and  behavior  of  the  egg  will  be  discussed 
under  fertilization,  but  the  synergids  present  certain  peculiari- 
ties that  may  be  considered  here.  The  name  "  synergid,"  given 

by  Strasburger,  has  proved  most  ap- 
propriate, for  it  is  usually  both  a  nu- 
tritive and  mechanical  "  helper  "  in 
the  process  of  fertilization,  although 
it  does  not  "  serve  to  convey  the  fer- 
tilizing substance  from  the  pollen- 
tube  to  the  oosphere,"  as  once  sup- 
posed. The  two  synergids  follow  the 
configuration  of  the  apex  of  the  sac, 
which  is  usually  rounded,  and  hence 
they  are  pyriform  for  the  most  part. 
In  certain  cases,  however,  the  sac  be- 
comes pointed  or  even  much  elon- 
gated, and  the  synergids  develop 
beak-like  extensions  of  more  or  less 
prominence,  which  in  many  cases 

have  been  found  to  pierce  the  wall  of  the  embryo-sac  and 
extend  into  the  micropyle  (Fig.  44).  Occasionally  the  beak& 
show  delicate  longitudinal  striations,  and  were  called  by  Schacht 
the  "  filiform  apparatus."  Such  beak-like  extensions  of  the 
sac  and  synergids  are  usually  associated  with  narrow  and  long 
micropyles,  and  doubtless  are  of  assistance  in  the  progress  of 
the  pollen-tube.  ,~  Among  the  Monocotyledons  they  are  by  na 
means  so  common  as  among  Dicotyledons,  but  are  well  scat- 
tered among  the  families.  For  example,  they  occur  in  Sorghum 
and  Zea  (Guignard71),  Eichhornia  (Smith53),  Crocus  (Hof- 
meister  *),  Romulea  (Ferraris  12°),  and  Gymnadenia  (Marshall- 
Ward  7),  and  doubtless  in  others.  Among  the  Archichlamydeae 
they  are  more  numerous,  having  been  noted  in  Salix  (Chamber- 
lain 46),  Quercus  (Conrad  78),  Santalum,  Polygonum  (Strasbur- 
ger5),  Hepatica  (Mottier  36),  Tlialictrum  (Overton  110),  Silene 
and  Capsella  (Guignard  12),  and  becoming  very  long  in  Euphor- 
bia (Miss  Lyon54)  and  Slum.  They  are  even  more  common 
among  the  Sympetalae,  a  fact  perhaps  to  be  associated  with  the 


FIG.  43.  —  Polygonum  divarica- 
tum.  Embryo-sac  ready  for 
fertilization :  showing  syner- 
gids with  "  filiform  appara- 
tus," egg,  and  primary  endo- 
sperm nucleus ;  x  540. — After 

STRASBURGER.6 


THE  FEMALE  GAMETOPHYTE 


95 


very  heavy  integument.  They  have  b£en  noted,  for  example,  in 
Campanula,  Jasminum,  and  Salvia  (Guignard  12),  and  in  almost 
all  the  species  of  Compositae  investigated.  In  Calendula  lusi- 
tanica  Billings100  reports  a  very  conspicuous  synergid  hausto- 
rium,  the  synergids  developing  into  the  micropyle  and  much 
enlarging.  Synergid  haustoria  have  been  reported  in  other 
forms,  which  are  probably  outgrowths  of  the  sac.  The  behavior 
of  the  synergids  of  Trapella,  as  described  by  Oliver,21  is  re- 
markable, after  fertilization  increasing  much  in  size,  and  in 
the  mature  seed  forming  a  conspicuous  tubercle-like  body 
(Fig.  32). 

It  has  been  generally  assumed  that  the  polar  nuclei  fuse  as 
soon  as  formed,  which  is  perhaps  generally  true.  If  the  time 
of  fusion  be  related  to  the  act  of  fertilization,  however,  it  will 
be  found  to  vary  from  before  pollination  to  long  after  fertiliza- 
tion, and  in  some  cases,  already  mentioned  (Lemna,  Gymnade- 
nia,  Balanophora,  Anlennaria  alpina),  the  polar  nuclei  seldom  if 


FIG.  44. —  4,  Salix  petiolaris,  upper  end  of  embryo-sac  soon  after  fertilization :  />,  pollen- 
tube  ;  s,  synergic! ;  the  synergids,  which  are  beaked  and  have  the  "  filiform  appara- 
tus," have  broken  through  the  embryo-sac  into  the  micropyle ;  x  694.  B,  S.  glau- 
cophylla,  synergids  not  disintegrating  after  the  formation  of  the  embryo;  polar 
nuclei  have  not  fused  ;  x  694.— After  CHAMBERLAIN.*' 


ever  fuse.  In  this  connection  it  may  be  noted  that  there  is  no 
antipodal  polar  nucleus  in  Limnocharis  (Hall109)  and  Helosis 
(Chodat  and  Bernard  83).  Fusion  of  the  polar  nuclei  at  any 
time  from  before  pollination,  as  in  Eichhornia  (Smith53),  to 
the  moment  of  sexual  fusion,  as  in  LiUum,  may  be  regarded  as 
normal.  Later  fusion  of  the  nuclei  has  been  noted  in  the 


/ 


96  MORPHOLOGY  OF  ANGIOSPERMS 

Xvctaginaceae  and  Conyza  by  Guignard,12  in  Alchemilla  by 
Murbeck,94  in  Sium,  in  which  case  they  are  relatively  small  and 
remain  near  one  another  in  a  parietal  position  until  the  em- 
bryo-sac has  become  much  enlarged,  in  Nicotiana  by  Guig- 
nard,107 and  in  Juglans  nigra  by  Karsten,115  in  which  there 
may  be  no  fusion.  In  this  connection  the  recent  experiments 
of  Shibata  122  upon  Monotropa  uniflora  are  of  interest.  He 
found  that  the  polar  nuclei  may  fuse  in  the  absence  of  pollina- 
tion, but  that  fusion  is  hastened  by  pollination.  For  example, 
when  pollination  occurs  the  polar  nuclei  fuse  in  about  five  days, 
but  when  pollination  is  prevented  the  fusion  does  not  occur  for 
ten  days  or  more. 

It  seems  to  be  generally  true  that  the  polar  nuclei  either 
fuse  in  contact  with  the  egg,  as  observed  by  Guignard  12  in 
Eriobotrya,  Cuphea,  Nicotiana,107  and  other  forms,  or  the 
fusion-nucleus  migrates  to  that  position  just  before  fertiliza- 
tion, as  in  Tricyrtis  (Ikeda100),  or  after  fertilization,  as  re- 
ported by  Balicka-IwanowTska  68  for  the  Scrophulariaceae  and 
allied  families.  The  last  observer  suggests  that  this  position  of 
the  primary  endosperm  nucleus  has  to  do  with  the  nutrition  of 
the  fertilized  egg ;  but  the  case  of  Tricyrtis  suggests  a  function 
during  fertilization.  It  is  certainly  true  that  in  most  cases 
this  nucleus  is  finally  either  in  contact  with  the  egg  or  very 
near  to  it.  In  Sagittaria  (Schaffner  47)  and  Potamogeton 
(Holferty97)  the  polar  nuclei  fuse  in  the  antipodal  end  of  the 
sac,  but  at  the  first  division  of  the  fusion-nucleus  one  daughter- 
nucleus  moves  towrard  the  egg-apparatus.  The  evidence  seems 
to  show  that  the  polar  nuclei  and  the  fusion-nucleus  have 
freedom  to  "  wander  "  through  the  sac,  and  that  there  is  at  some 
time  a  relation  in  position  to  the  egg.  For  example,  in  Tri- 
cyrtis Ikeda  106  has  described  the  fusion-nucleus  as  passing  first 
to  the  antipodals,  and  then  passing  to  the  egg  just  before  fer- 
tilization. 

The  antipodal  cells  are  either  naked  or  invested  by  walls, 
and  are  exceedingly  variable  as  to  their  arrangement,  number, 
and  persistence.  The  ordinary  statement  that  the  number  of 
cells  is  limited  to  the  three  primary  ones,  and  that  they  are  more 
or  less  ephemeral,  taking  no  part  in  the  activities  of  the  embryo- 
sac,  has  proved  to  be  far  from  true  in  the  majority  of  cases 
investigated.  It  is  impossible  to  classify  them  as  ephemeral 


THE  FEMALE  GAMETOPHYTE  97 

and  inactive,  or  relatively  persistent  and  active,  for  the  grada- 
tions between  these  two  extreme  conditions  are  complete. 
is  noticeable,  however,  that  the  two  conditions  are  apt  to  be 
characteristic  of  families,  and  that  the  most  extensive  develop- 
ment of  the  antipodal  cells  is  found  in  comparatively  few 
families. 

It  is  needless  to  attempt  to  give  a  complete  list  of  those 
families  in  which  the  antipodal  cells  are  ephemeral,  disorgan- 
izing with  more  or  less  rapidity,  and  apparently  taking  no  part 
in  the  activities  of  the  embryo-sac.  The  following  data  will 
serve  to  illustrate  that  this  condition  is  found  in  groups  of 
every  rank.  Among  Monocotyledons,  ephemeral  antipodals 
are  found  in  Typhaceae,  Xaiadaceae  (Potamogeton),  Alisma- 
ceae,  Pontederiaceae,  Liliaceae  (except  Ornithogalum),  Sci- 
tamineae,  and  Orchidaceae;  among  Archichlamydeae,  in  Sau- 
ruraceae,  Salicaceae,  probably  Casuarinaceae,  Cupuliferae, 
Loranthaceae  (Loranthus),  Caryophyllaceae,  Cruciferae,  Saxi- 
fragaceae,  Leguminosae,  Euphorbiaceae,  Aceraceae,  Cactaceae, 
Onagraceae,  and  Urnbelliferae ;  and  among  the  Sympetalae,  in 
Oleaceae,  Bignoniaceae,  Pedaliaceae,  Scrophulariaceae  and 
their  allies,  and  certain  Rubiaceae.  A  certain  amount  of  varia- 
tion in  these  families  has  been  found,  as  will  be  noted  later, 
and  doubtless  much  more  will  be  found  as  other  species  are 
investigated.  It  will  also  be  noted  that  this  condition  is 
probably  not  so  prevalent  in  the  Sympetalae  as  in  the  other 
groups. 

In  those  antipodal  cells  that  function  more  or  less  there  is 
every  degree  of  prominence.  It  should  also  be  noted  that  antip- 
odals of  the  same  sac  often  differ  very  much  in  prominence.  For 
example,  in  Lilium  the  innermost  antipodal  is  often  the  most 
prominent,  in  Nicotiana  (Guignard  107)  they  are  often  unequal 
in  size,  among  the  Galieae  (Lloyd  105)  one  of  the  three  is  much 
elongated,  and  among  the  Compositae  the  one  nearest  the  cha- 
laza  is  often  very  much  enlarged  (Fig.  47).  The  simplest  cases 
are  those  in  which  the  cells  do  not  grow  very  large  or  divide, 
but  by  their  prominence  and  persistence  indicate  that  they  are 
taking  some  part  in  the  activities  of  the  embryo-sac,  as  in 
Vise  urn,  Xyctaginaceae,  Ruta,  Poly  gala,  Borago,  Salvia,  Nico- 
tiana, and  SarcodeSj  as  well  as  certain  members  of  families 
characterized  by  a  striking  development  of  the  antipodal  cells. 


98  MORPHOLOGY   OF  ANGIOSPERMS 

In  other  instances  the  activity  of  the  antipodal  cells  is 
shown  by  their  great  increase  in  size  and  usually  multinucleate 
condition,  and  also  by  their  more,  or  less  extensive  division. 
Among  the  Monocotyledons,  the  Sparganiaceae,  Gramineae, 
and  Araceae  are  conspicuous  for  their  strongly  developed  antip- 
odal cells.  In  Sparganium  simplex  Campbell  63  describes  the 


FIG.  45.— Sparganium  simplex.     Lower  end  of  embryo-sac  showing  a  large  mass  of 
antipodal  cells. — After  CAMPBELL." 

antipodal  cells  as  at  first  very  small,  but  immediately  after 
fertilization  they  enlarge  to  several  times  their  original  size, 
their  nuclei  dividing.  Finally,  a  conspicuous  hemispherical 
mass  of  100  to  150  uninucleate  cells  is  formed,  at  this  stage  the 
endosperm  having  hardly  at  all  developed  (Fig.  45).  The 
strong  development  of  antipodal  cells  among  the  Gramineae 
has  long  been  known,  Fischer  6  having  reported  in  1880  that 
each  antipodal  cell  of  Ehrarta  panicea  divides  once,  and  of 
Alopecurus  pratensis  three  or  more  times.  More  recently 
Cannon 86  found  in  Avena  fatua  that  the  antipodal  cells  be- 
come thirty-six  or  more  in  number  before  fertilization,  and 
begin  to  disorganize  with  the  beginning  of  endosperm  devel- 
opment. Westermaier  23  has  described  a  growth  of  antipodal 
tissue  in  Zea  and  other  grasses  before  fertilization,  and 
Guignard  90  has  found  as  many  as  twelve  multinucleate  cells 
in  the  much  narrowed  antipodal  end  of  the  embryo-sac  of 
Zea.  It  is  of  interest  to  note  in  this  connection  that  in  1882 
the  same  investigator12  found  in  Cornucopiae  undivided  but 
prominent  and  often  binucleate  antipodal  cells.  Among  the 
Araceae  Campbell  75  states  that  there  is  a  general  tendency  for 
the  antipodals  to  develop  strongly,  often  dividing  and  forming 
a  tissue,  and  in  Lysichiton  Jcamtschatcense  the  same  observer  63 
finds  that  at  the  time  of  fertilization  the  antipodal  nuclei  have 


THE  FEMALE  GAMETOPHYTE 


increased  remarkably  in  size,  and  after  fertilization  the  cells 
increase  rapidly  and  divide,  forming  a  group  of  eight  or  more 
cells  with  remarkably  large  nuclei.  In  addition  to  these  three 
monocotyledonous  families,  a  prominent  antipodal  region  has 
been  found  in  Triglochin  maritima  (Hill76),  in  which  there 
are  three  to  fourteen  cells ;  very  large  but  undivided  antipodals 
have  been  found  in  Lilaea  (Campbell56),  Commelina  (Guig- 
nard12),  Ornithogalum,  Gladiolus,  and  Crocus  (Mottier36), 
Narcissus  and  Iris  (Guignard  12),  and  Romulea  (Ferraris  12°)  ; 
and  Ikeda  106  reports  that  in  Tricyrtis  the  antipodals  fill  up 
the  "  chalazal  protuberance,"  become  elongated  with  it,  and 
reach  their  maximum  length  just  before  fertilization. 

Among  the  Archichlamydeae,  the  Ranunculaceae  are  espe- 
cially characterized  by  the  activity  of  the  antipodal  cells,  shown 
both  by  their  great  size  and 
multinucleate  condition,  and 
also  by  their  divisions.  We 
have  records  of  twelve  genera, 
and  in  all  of  them  the  antipo- 
dals are  conspicuous.  In  1879 
Strasburger  5  reported  the  an- 
tipodals of  Myosurus  as  very 
prominent,  and  in  1882  Guig- 
nard 12  described  the  antipodals 
of  Erianiliis  as  large,  those  of 
Clematis  as  very  large  and  bi- 
nucleate,  and  those  of  Hepatica 
as  forming  a  great  group  and 
becoming  multinucleate  after 
fertilization.  In  1890  Wester- 
maier  23  reported  large  antipo- 
dals in  Ranunculaceae,  among 
them  NifjeUa;  and  in  1895 
Mottier  36  investigated  a  num- 
ber of  genera  and  described  the 
antipodals  of  Delphinium  tri- 
corne  as  very  large,  growing 
with  the  embryo-sac,  and  persisting  till  after  fertilization; 
those  of  Caltlia  palustris  as  large,  pyriform,  and  multinu- 
cleate; those  of  Aquilegia  canadensis  as  growing  enormously 


FIG.  46. — Aconitum  Napellus.  Longitudi- 
nal section  of  embryo-sac  after  fertili- 
zation, showing  the  three  very  large 
antipodals :  nuclei  of  endosperm  in  mi- 
tosis; x  45. — After  OSTERWALDER.«° 


100 


MORPHOLOGY  OF  ANGIOSPERMS 


before    and    after    fertilization    and   becoming   multinucleate ; 

those  of  various  species  of  Ranunculus,  Anemonella,  and  Thal- 

ictrum  dioicum  as  very  large;  and 
those  of  Hepatica  as  growing  very 
much  until  after  fertilization.  Since 
then  Overton  110  has  found  that  the 
antipodals  of  Thalictrum  purpuras- 
cens  become  remarkably  large,  reach- 
ing the  center  of  the  sac ;  Miss 
Dunn 89  has  reported  that  in  Del- 
phinium exaltatum  three  very  large 
antipodals  persist  even  in  the  oldest 
seeds  with  no  indication  of  degen- 
eration; Miss  Lyon  has  noted  as- 
many  as  twenty-five  antipodal  cells 
in  Hepatica ;  and  Osterwalder  60  has 
figured  exceedingly  large  antipodals 
in  Aconitum  Napellus  (Fig.  46). 
The  whole  family  is  characterized, 
therefore,  by  the  activity  of  its  an- 
tipodal cells,  exhibited  more  by  their 
great  increase  in  size  than  by  divi- 
sion. Among  the  Amentiferae  Miss 
Benson 31  reports  a  row  of  six  or 
more  superposed  antipodals  in  the 
very  narrow  antipodal  end  of  the 
sac  in  Castanea  vulgaris,  the  lowest 
one  being  figured  as  the  largest  and 
multinucleate,  the  whole  structure 
resembling  the  antipodal  region  of 
many  Compositae.  Around  the  base 
of  this  elongated  antipodal  region 
there  are  developed  such  tr  ache  id- 
like  cells  as  occur  in  the  nucellus 


FIG.  47. — Aster  novae-angliae.  Longitudinal  sec- 
tion of  embryo-sac  just  before  fertilization^; 
m,  micropyle ;  «,  synergid ;  o,  oosphere ;  e,  en- 
dosperm nucleus ;  2,  jacket;  A, lower  antipodal 
cell;  four  other  antipodal  cells  shown,  the 
upper  with  four  nuclei  and  the  others  with  two ; 

X    407.— After  CHAMBERLAIN.85 


THE  FEMALE  GAMETPfrtrTE  :''*\"   101 


of  Casuarina,  but  in  this  latter 
instance  they  are  derived  from 
mother-cells.  Other  Archichlam- 
ydeae  with  active  antipodals  are 
Heckeria  (Johnson  114),  in  which 
they  are  sometimes  six  to  eight  in 
number;  Asarum  (Hofmeister  2), 
in  which  they  are  very  long,  ex- 
tending at  fertilization  from  one- 
third  to  one-half  the  length  of  the 
embryo-sac,  and  sometimes  divi- 
ding; Jeffersonia  diphylla  (An- 
drews37), in  which  they  become 
about  one-half  as  long  as  the 
embryo-sac;  Eriobotrya  (Guig- 
nard  12),  in  which  they  are  large; 
and  Anoda  (Guignard 12),  in 
which  they  are  prominent  and 
often  binucleate. 

Among  the  Sympetalae  the 
Compositae  are  especially  note- 
worthy for  the  extensive  develop- 
ment of  the  antipodal  region  (Fig. 
47).  In  this  family  the  chalazal 
end  of  the  elongated  sac  is  very 
narrow  and  the  antipodals  are 
superposed.  In  a  number  of 
cases,  as  in  Doronicum,  Petasites, 
and  Taraxacum,  there  are  usually 
only  three  antipodals,  but  they 
remain  active ;  while  in  Tussila- 
go  (Guignard  12)  there  are  usual- 
ly four;  in  Senecio  (Mottier29) 
two  to  six;  in  Silphium  (Mer- 
rell77)  three  to  eight;  in  Conyza 
(Guignard12)  eight  to  ten;  in 
Aster  novae-anyliae  (Chamber- 
lain35) three  to  thirteen;  and  in 
Antennaria  (Juel57)  they  con- 
tinue to  divide  until  quite  a  tis- 


o.  48. — A^  Sherardia  arvenvis.  Em- 
bryo-sac before  fertilization;  low- 
er antipodal  acting  as  an  hausto- 
rium.  -5,  Callipeltis  cucullaria, 
showing  lower  antipodal  still  act- 
ive after  embryo  and  endosperm 
are  considerably  advanced. — After 

LLOYD.106 


102  MORPHOLOGY  OF  ANGIOSPERMS 

sue  >s^  formed;  (Fig,  41)*'  .  Tliis  record  indicates  that  the  divisions 
are  variable  in  number  even  in  the  same  species,  and  it  may 
be  noted  in  this  connection  that  while  Schwere  42  states  that 
there  are  only  three  antipodals  in  Taraxacum,  Hegelmaier 9 
had  previously  reported  four  or  five,  and  more  than  three  have 
been  observed  frequently  in  this  laboratory.  In  many  of  these 
cases  all  the  cells  usually  contain  two  or  more  nuclei,  and  the 
end  cell  toward  the  chalaza  often  becomes  vesicular  and  multi- 
nucleate,  breaking  through  the  sac  and  encroaching  upon  the 
chalazal  tissue.  It  seems  to  be  clear  that  in  the  Compositae 
this  development  of  antipodals  is  practically  an  aggressive  haus- 
torium  for  the  embryo-sac;  while  in  the  Ranunculaceae  the 
antipodals  doubtless  serve  as  an  haustorium,  but  do  not  invade 
the  neighboring  tissue.  Certain  Rubiaceae  also  contain  active 
antipodals,  since  Lloyd  67  lias  found  that  in  Vaillantia  hispida 
while  two  of  the  antipodals  are  insignificant,  the  third  is  very 
prominent  and  remains  active  for  a  long  time.  The  same  au- 
thor 105  has  more  recently  found  the  same  to  be  true  of  the 
Galieae  (Fig.  48),  and  he  also  has  found  four  to  ten  antip- 
odals in  'Diodia  virginiana.  Balicka-Iwano\vska 68  has  also 
noted  enlarging  and  persistent  antipodals  in  Plantaginaceae  and 
Campanulaceae,  and  their  division  in  Dipsaceae  as  in  the  Com- 
positae. In  Asclepias,  although  three  active  antipodals  are 
usual,  Frye  118  has  observed  compact  antipodal  tissue  consisting 
of  seven  or  eight  cells;  and  in  A.  Cornuti  he  has  noted  the 
occurrence  of  tracheid-like  cells  at  the  base  of  the  embryo-sac, 
such  as  occur  in  Casuarina  and  Castanea. 

There  seems  to  be  no  reason  to  question  the  ordinary  view 
that  the  antipodal  cells  are  vegetative  cells  of  the  gametophyte. 
Their  polarity  as  contrasted  with  that  of  the  egg-apparatus, 
and  their  behavior  when  they  function  confirm  it.  The  occa- 
sion for  their  activity  seems  to  be  to  supply  the  embryo-sac  with 
nutritive  material  absorbed  from  without  at  a  time  when  the 
endosperm  has  not  been  organized  or  other  means  of  obtain- 
ing nutrition  are  not  available.  In  Monotropa  uniflora  Shi- 
bata  122  has  found  that  the  three  small  antipodals  disintegrate 
after  fertilization,  but  that  when  fertilization  is  prevented  they 
may  enlarge  enormously  and  fill  a  considerable  portion  of  the 
sac.  The  character  of  the  active  antipodals  among  the  more 
primitive  Monocotyledons  and  in  the  Ranunculaceae  may  be 


THE  FEMALE  GAMETOPHYTE  103 

regarded  as  indicating  a  primitive  condition  of  the  nutritive 
ti— no  in  the  female  gametophytes  of  Angiosperms;  but  the 
antipodals  of  many  of  the  Compositae  are  organized  into  an 
jii:i:Ti —  ive  haustorium  which  can  only  be  regarded  as  a  very 
specialized  organ. 

The  enlargement  of  the  embryo-sac  and  the  nature  of  its 
development,  both  before  and  after  fertilization,  are  extremely 
varied.  The  enlargement  is  directly  related  to  the  digestion 
of  the  contiguous  tissue.  In  a  few  cases  this  destruction  is  not 
extensive,  and  more  or  less  of  the  nucellar  tissue  is  permanent 
(perisperm)  and  is  used  for  the  storage  of  reserve  food,  as  in 
the  Scitamineae,  Piperaceae,  Chenopodiaceae,  Phytolaccaceae, 
Caryophyllaceae,  Xymphaeaceae,  etc.  In  most  cases,  however, 
the  destruction  of  the  nucellar  tissue  is  complete  to  the  integu- 
ment, and  even  that  is  sometimes  involved,  as  in  Allium  odo- 
/•////<,  certain  orchids,  and  Astilbe  (Webb111).  Frequently  the 
tissue  at  the  apex  of  the  nucellus  remains  as  a  cap  on  the  em- 
bryo-sac, as  in  Arisaema  (Mottier27)  and  other  Araceae, 
Lemna  (Caldwell 62),  Liliaceae,  Silphium  (Merrell77),  and 
many  other  forms,  and  this  is  frequently  accompanied  by  more 
or  less  elongation  and  even  division  of  the  capping  cells. 

Frequently  a  definite  nutritive  jacket  invests  the  embryo- 
sac,  consisting  of  one  or  more  layers  of  cells  with  deeply  stain- 
ing contents  (Figs.  47,  50).  For  the  most  part  this  is  a  single 
layer  derived  from  the  integument,  but  in  Armeria  it  is  derived 
from  the  nucellus,  and  in  Erodium  one  layer  is  derived  from 
the  nucellus  and  the  other  from  the  integument.  This  jacket 
has  been  called  a  tapetum,  and  such  it  is  in  function.  In  using 
the  term,  however,  there  is  danger  of  confusing  it  with  the 
tapetum  of  ordinary  sporogenous  tissue.  This  jacket  has  been 
definitely  observed  as  conspicuous  in  Helosis  (Chodat  and 
Bernard83),  Sium,  many  Scrophulariaceae  (Balicka-Iwanow- 
ska68),  Campanula  (Barnes18),  Stylidaceae  (Burns85),  and 
certain  Compositae,  and  by  Billings  10°  in  numerous  sympeta- 
lous forms,  among  the  most  conspicuous  being  Lobelia,  Primu- 
laceae  (except  Le  pi  o  siphon},  Linum,  Forsythia,  Amsonia, 
Menyanthes,  Polemoniaceae,  Myoporum,  Globularia,  Scaevola, 
Calendula,  etc. 

In  many  cases  the  micropylar  end  of  the  sac  destroys  all 
of  the  nucellar  tissue  capping  it,  and  protrudes  more  or  less 


104 


MORPHOLOGY  OF  ANGIOSPERMS 


into  the  micropyle,  as  in  Hemerocallis,  Crocus,  Gladiolus, 
Eomulea  (Ferraris  12°),  Alchemilla  (Murbeck94),  in  which  the 
sac  pushes  through  to  the  tegumentary  tissue  closing  the  micro- 
pyle, Medicago,  Torenia  asiatica  (Strasburger  5),  Labiatae, 
Vaillantia  (Lloyd67),  Diodia  and  the  Galieae  (Lloyd105),  and 
many  other  forms.  In  Vaillantia  the  mother-cell  migrates  into 
the  micropyle  and  develops  there. 

While  ordinarily  the  embryo-sac  is  relatively  broad   and 
rounded  at  its  micropylar  extremity,  this  is  by  no  means  so 

commonly  true  of  the  antipodal 
end.  If  the  antipodals  are  ephem- 
eral, the  growth  of  the  antipodal 
region  is  frequently  checked  after 
the  first  division  of  the  megaspore 
nucleus,  and  through  the  growth  of 
the  rest  of  the  sac  it  becomes  a 
very  small  pocket,  as  in  Typliay 
Potamogeton,  Sagittaria,  certain 
Gramineae,  Pontederia,  Lilium, 
Oenothera,  etc.  (Fig.  79).  It  is 
generally  true  that  the  antipodal 
region  of  the  sac  is  narrower  than 
the  micropylar,  but  its  growth  is 
not  often  checked  so  completely 
and  so  early  as  in  the  cases  cited. 

In  other  cases,  the  antipodal 
region  of  the  sac  grows  very  active- 
ly, elongating  toward  the  chalazal 
region  and  penetrating  it  more  or 
less  deeply,  resulting  in  a  very  nar- 
row and  elongated  sac.  Such  an 
antipodal  region  must  be  regarded 
as  an  haustorium  that  digests  and 
absorbs  its  way  into  the  chalazal  tis- 
sue. Illustrations  of  this  are  very  numerous,  as  in  Gramineae, 
Tricyrtis  (Ikeda106),  Scitamineae,  Saururaeeae,  Loranthaceae, 
Polygalaceae,  Lythraceae,  Aceraceae,  and  most  Sympetalae. 
In  penetrating  the  chalaza  the  antipodal  tip  usually  remains 
narrow,  but  in  Saururus  (Johnson87),  Scitamineae  (Hum- 
phrey40), Cuphea  (Guignard  12),  Campanula  (Barnes18),  etc., 


FIG.  49. — Saururus  cernuus.  Longi- 
tudinal section  of  embryo-sac; 
after  the  first  division  of  the  en- 
dosperm nucleus  the  micropylar 
cell  has  given  rise  to  endosperm 
tissue,  while  the  other  cell  has 
become  a  large  vesicular  hausto- 
rium.— After  JOHNSON.W 


THE  FEMALE  GAMETOPHYTE  105 

it  has  been  observed  to  enlarge  more  or  less  abruptly,  forming 
a  bulbous  chalazal  haustorium.  In  Canna  indica  this  becomes 
much  larger  than  the  rest  of  the  embryo-sac;  and  in  Saururus 
i-'  muus  Johnson  87  describes  the  embryo-sac  as  elongating  rap- 
idly, broadening  below,  the  upper  part  remaining  narrow,  the 
completed  sac  resembling  a  long-necked  flask  (Fig.  49). 

In  addition  to  the  various  forms  of  haustorial  apparatus 
described  above  as  developed  in  connection  writh  the  embryo-sac, 
certain  extreme  cases  deserve  special  mention.  It  has  long 
been  known  that  among  the  Santalaceae  (Santalum,  Thesium, 
Osyris,  etc.)  the  embryo-sac  develops  a  micropylar  tube  that 
passes  through  the  micropyle  and  enters  the  cavity  of  the  ovary, 
and  that  in  some  of  them  (Thesium,  etc.)  there  is  also  an  antip- 
odal tube  (see  Guignard17).  These  remarkable  tubular  or 
vermiform  haustoria  obtain  nutritive  material  beyond  the  ovule. 
Later,  Johnson  22  described  in  detail  the  haustorial  apparatus 
of  Myzodendron,  another  genus  of  Santalaceae.  The  young  sac 
is  broad  above  and  narrowed  toward  the  antipodal  end.  After 
fertilization  the  antipodal  region  develops  rapidly,  penetrates 
the  chalaza,  enters  the  placental  axis,  and  curving  passes  down 
it  to  the  base  of  the  flower,  where  its  tip  dilates  and  becomes 
embedded  in  the  "  vascular  cup  "  formed  by  the  three  diverging 
carpellary  bundles.  Rigidity  is  given  to  this  remarkably  elon- 
gated tube  by  numerous  cross-walls,  but  these  are  lacking  in  the 
placental  region. 

Among  the  Amentiferae  (Miss  Benson31)  vermiform  caeca 
are  often  sent  out  from  the  embryo-sac.  In  Fagus  sylvatica 
this  tubular  outgrowth  penetrates  to  the  base  of  the  nucellus, 
the  primary  endosperm  nucleus  passing  into  it,  but  not  the 
antipodals,  which  are  anchored  by  thick  walls.  In  Costarica 
vulgaris  the  caecum  develops  from  the  side  of  the  sac  just  above 
the  narrow  antipodal  prolongation,  is  entered  by  the  endosperm 
nucleus,  and  passes  down  between  the  nucellus  and  the  integu- 
ment. In  Carpinus  Betulus  the  chalazal  region  is  sometimes 
riddled  by  the  long  caeca  from  the  several  embryo-sacs ;  and  in 
Corylus  Avellana  a  short  caecum  appears  after  fertilization. 

In  Casuarina,  as  shown  by  Frye,139  a  conspicuous  vermi- 
form caecum  is  developed  much  as  among  the  Amentiferae. 
From  the  antipodal  extremity  of  the  sac  a  long  tube  penetrates 
the  chalazal  region,  into  which  the  endosperm  nucleus  passes 


106  MORPHOLOGY  OF  ANGIOSPERMS 

and  sometimes  the  antipodals.  This  haustorial  tube  was  ob- 
served to  begin  its  development  at  different  stages  in  the  history 
of  the  sac,  sometimes  being  evident  in  the  two-nucleate  stage 
of  the  sac,  sometimes  not  having  begun  in  the  seven  or  eight- 
nucleate  stage. 

One  of  the  strangest  cases  is  that  of  Trapella,  as  described 
by  Oliver.21  In  this  the  innermost  megaspore  of  a  row  of  four 
becomes  extremely  elongated,  penetrates  the  chalaza,  and 
divides  longitudinally,  the  tAvo  cells  being  very  active,  as  indi- 
cated by  their  contents  and  numerous  starch  grains.  In  this 
form  the  synergids  enlarge  and  persist  on  the  apex  of  the  sac 
(Fig.  32). 

Among  the  Scrophulariaceae,  such  as  Pedicularis,  Rhinan- 
thus  and  its  allies,  etc.,  Tulasne,  Hofmeister,  Tschirch,  Schlot- 
terbeck,  and  others  have  described  the  numerous  vermiform 
tubes  that  develop  from  the  embryo-sac  and  "  ruminate  "  the 
integument  and  destroy  its  tissue,  although  they  did  not  recog- 
nize their  origin ;  and  similar  tubes  have  been  found  in  certain 
Labiatae.  Recently  Balicka-Iwanowska  68  has  investigated  the 
embryo-sacs  of  many  Scrophulariaceae,  as  well  as  other  allied 
Sympetalae,  and  has  discovered  a  remarkably  constant  occur- 
rence of  haustorial  outgrowths  from  the  sac  at  both  micropylar 
and  chalazal  ends,  filled  in  later  by  endosperm  cells.  The 
common  case  is  for  the  broad  micropylar  end  of  the  sac  to  de- 
velop four  prongs,  and  for  the  narrower  chalazal  end  to  fork, 
as  seen  not  merely  among  Scrophulariaceae,  but  also  among 
Utriculariaceae,  Pedaliaceae,  and  Plantaginaceae.  The  devel- 
opment of  these  haustoria  is  related  to  the  thickness  of  the 
integument,  which  in  these  groups  seems  to  be  a  source  of  nutri- 
tive supply.  There  are  all  stages  in  the  development  of  the 
haustoria,  but  the  general  tendency  in  this  region  of  the  Sympet- 
alae is  very  marked.  A  striking  case  is  that  of  the  well-known 
Torenia  asiatica,  mentioned  above,  in  which  the  sac  does  not 
develop  outgrowths,  but  protrudes  bodily  beyond  the  micropyle, 
touching  the  funiculus,  and  even  reaching  the  ovary  wall.  All 
of  these  haustorial  outgrowths  are  supplied  with  active  endo- 
sperm cells  or  nuclei. 

It  is  stated  that  all  species  of  Campanulaceae  (Balicka- 
Iwanowska 68),  Lobeliaceae  (Billings100),  and  Stylidaceae 
(Burns  85)  develop  both  micropylar  and  chalazal  haustoria,  and 


FIG.  50.— A,  Globularia  cordifolia,  the  micropylar  end  of  the  embryo-sac  has  grown 
out  into  an  extensive  haustorium  furnished  with  nuclei  from  the  endosperm;/, 
funiculus ;  after  BILLIXGS.IO°  B,  Plantago  lanceolata,  longitudinal  section  of  ovule 
after  embryo  is  somewhat  advanced,  showing  extensive  haustorial  system;  after 
BALICKA-IWANOWSKA.««  (7,  Stylidium  squamellosum,  embryo-sac  after  second 
division  of  endosperm  nucleus ;  e,  egg ;  j9,  pollen-tube ;  after  BuRus.85  Z>,  Byblis 
gigantea,  longitudinal  section  of  seed  with  branching  haustoria  in  both  micropylar 
and  antipodal  regions ;  A,  haustorium ;  g^  embryo ;  «,  endosperm  ;  after  Lx>*G.91 

107 


108 


MORPHOLOGY  OF  ANGIOSPERMS 


that  often  finger-like  processes  are  put  out  at  the  side  or  base 
of  the  sac,  extending  toward  the  vascular  bundles ;  and  in  Sty- 
lidaceae,  immediately  after  the  entrance  of  the  pollen-tube,  the 
micropylar  part  of  the  embryo-sac  grows  out  into  an  enormous 
haustorium  much  larger  than  the  rest  of  the  sac  (Fig.  50).  As 
a  result  of  his  investigations  of  Polypompholyx  and  Byblis, 
Lang  91  not  only  discovered  conspicuous  haustoria,  but  used  this 
character,  along  with  others,  such  as  the  nucellus  with  a  single 

row  of  axial  cells,  the  tapetum  de- 
rived from  the  single  integument, 
and  the  united  petals,  to  remove 
these  genera  from  the  archichlamy- 
deous  Droseraceae  to  the  sympetalous 
Lentibulariaceae. 

The  whole  subject  of  the  mecha- 
nism for  the  nutrition  of  the  embryo- 
sac  deserves  more  detailed  attention 
than  it  has  received.  In  his  study  of 
the  fleshy  plants,  D' Hubert,33  on  the 
basis  of  the  appearance  and  disap- 
pearance of  starch,  concludes  that  the 
antipodals  nourish  the  sac  before  fer- 
tilization, the  synergids  nourish  the 
nuclei  of  the  pollen-tube  and  then 
the  nucleus  of  the  egg  at  the  time  /  / 
of  fertilization,  and  the  polar  nuclei  I 
nourish  the  fertilized  egg  and  give 
rise  to  the  endosperm  (Fig.  51). 
Such  details  may  prove  true  for  the 
Cactaceae  and  other  fleshy  plants,* 
but  the  larger  field  is  to  be  traversed 
first,  which  embraces  all  of  the  mor- 
phological structures  used  in  obtaining  nutritive  supplies  for 
the  structures  within  the  embryo-sac,  both  before  and  after  fer- 
tilization. Just  what  mechanism  supplies  wrhat  structure  is  a 
subordinate  detail  and  very  difficult  to  prove,  besides  being  an 
exceedingly  improbable  division  of  labor  among  structures  so 

*  D'Hubert  concludes  that  starch  is  characteristic  of  fleshy  plants,  but 
there  is  a  large  display  of  starch  in  Astilbe  (Webb  1U)  and  Galium  (Lloyd  105), 
and  doubtless  in  many  other  non-fleshy  plants. 


FIG.  51.—Pkyllocactus.  Starch  dis- 
appearing from  antipodals  and 
accumulating  in  other  portions 
of  the  embryo-sac;  a,  antipo- 
dals ;  e,  egg-apparatus ;  />,  polar 
nucleus;  x  668.  — After  D'Hu- 

BERT.83 


THE  FEMALE  GAMETOPHYTE  109 

closely  associated.  From  the  data  more  or  less  scattered  through 
the  preceding  and  following  pages,  the  various  methods  by  which 
nutritive  supplies  are  brought  into  the  sac  may  be  grouped  to- 
gether as  follows,  although  the  subject  is  in  no  condition  as  yet 
for  satisfactory  organization. 

The  digestion  and  absorption  of  adjacent  tissue  by  the  en- 
larging sac  is  the  most  general  method  of  obtaining  nutritive 
supplies.  It  always  occurs  to  a  certain  extent,  and  often  is  the 
only  observed  method.  The  varying  amount  of  tissue  destroyed 
in  this  way  is  a  thing  of  common  observation. 

The  organization  of  a  definite  layer  or  layers  of  cells  about 
the  embryo-sac  in  its  later  stages,  which, we  have  called  the 
"  nutritive  jacket,"  has  not  been  reported  for  the  Monocotyle- 
dons, occurs  in  comparatively  few  Archichlamydeae,  while  it 
seems  to  be  common  among  the  Sympetalae.  For  the  origin 
and  occurrence  of  this  jacket  see  page  101.  Its  appearance  and 
function  is  that  of  a  tapetum,  and  there  seems  to  be  no  good 
reason  why  it  should  not  receive  the  name. 

Tracheid-like  cells  have  been  reported  in  the  nucellar  tissue 
of  Casuarina,  Castanea,  and  Asclepias,  but  this  meager  list  will 
doubtless  be  much  increased.  That  such  cells  are  connected 
with  a  nutritive  mechanism  seems  clear,  but  their  rare  and 
feeble  development  suggests  a  relic  of  an  efficient  ancestral 
mechanism.  The  recent  discovery  (Oliver  104)  of  a  Palaeozoic 
fern  with  certain  resemblances  to  the  Cycadofilices,  in  which 
tracheids  replaced  the  tapetum  in  the  sporangium,  may  be  an- 
other indication  of  the  former  somewhat  extensive  use  of  this 
special  form  of  mechanism.  Thick-walled  cells  often  appear 
in  the  chalazal  region,  especially  in  connection  with  the  pene- 
tration of  the  sac.  Some  are  as  hard  as  tracheids,  while  in 
other  cases  the  walls  have  become  mucilaginous  and  swollen. 
Similar  cells  also  occur  wherever  haustoria  invade  tissue  in  any 
other  region  of  the  ovule  or  outside  of  it. 

The  aggressive  penetration  of  the  chalazal  region  by  the 
elongation  of  the  antipodal  extremity  of  the  sac  is  very  common. 
This  definite  antipodal  haustorium  seems  to  be  nearly  always 
developed  when  a  more  or  less  prominent  mass  of  chalazal  tissue 
occurs.  Among  Monocotyledons  such  haustoria  are  recorded 
among  the  Gramineae,  Liliaceae,  and  Scitamineae ;  among  the 
Archichlamydeae  they  are  known  to  occur  among  the  Sauru- 


110  MORPHOLOGY  OF  ANGIOSPERMS 

raceae,  Loranthaceae,  Nymphaeaceae,  Polygalaceae,  Lythra- 
ceae,  and  Aceraceae,  while  they  seem  to  be  almost  universal 
among  the  Sympetalae.  In  most  cases  the  advancing  tip  re- 
mains narrow,  but  sometimes  it  becomes  enlarged,  in  certain 
cases  very  much  so.  For  example,  in  Canna  the  antipodal 
haustorium  becomes  a  bulbous  structure  larger  than  the  rest 
of  the  sac,  while  in  Saururus  the  narrow  micropylar  end  and 
the  bulbous  antipodal  haustorium  form  a  flask-shaped  sac. 

Among  the  Santalaceae  the  vermiform  haustoria  sent  from 
the  micropylar  extremity  of  the  sac  into  the  cavity  of  the  ovary 
have  been  noted.  Perhaps  the  most  remarkable  member  of  the 
family  in  this  regard,  however,  is  Myzodendron,  as  described 
above.  In  this  case  the  haustorium  is  really  an  extreme  devel- 
opment of  the  antipodal  extremity  of  the  sac,  but  the  elonga- 
tion is  so  excessive  that  it  has  been  included  in  this  rather  than 
in  the  preceding  category.  Among  the  Fagales  vermiform 
haustoria  are  more  or  less  prominent,  in  this  case  being  sent 
out  laterally  from  near  the  antipodal  extremity  and  penetrating- 
the  chalazal  tissue,  and  being  entered  by  the  endosperm  nucleus. 
Conspicuous  haustoria  of  this  type  are  reported,  as  noted  above, 
in  Fagus  and  Castanea,  while  in  Carpinus  the  chalazal  region 
is  sometimes  riddled  by  the  haustoria  from  the  several  sacs. 
Among  the  Sympetalae  vermiform  haustoria  are  common,  being 
well  known  among  Scrophulariaceae  and  their  allies,  as  well  as 
among  the  Campanulaceae,  Lobeliaceae,  and  Stylidaceae.  In 
addition  to  the  penetration  of  the  chalazal  tissue  by  haustoria 
from  the  antipodal  region  of  the  sac,  micropylar  haustoria  are 
often  sent  into  the  tissue  of  the  massive  integument.  Four 
such  micropylar  haustoria,  more  or  less  prominent,  and  always 
associated  with  active  endosperm  cells,  seem  to  be  common 
among  the  Scrophulariaceae.  'Such  haustoria  are  apt  to  be  coe- 
nocytic,  the  endosperm  consisting  of  large  and  densely  stain- 
ing nuclei  rather  than  of  walled  cells  as  in  other  parts  of  the 
sac.  The  haustorial  mechanism  is  evident  even  when  it  con- 
sists only  of  groups  of  active  endosperm  cells  in  contact  with 
definite  regions  of  the  sac  wall. 

In  this  connection  the  remarkable  case  of  Trapella  (Peda- 
liaceae)  may  be  mentioned,  in  which  the  innermost  megaspore 
of  the  linear  tetrad  becomes  modified  into  an  active  haustorium 
that  penetrates  the  chalazal  region  (Fig.  32). 


THE   FEMALE  GAMETOPHYTE  111 

The  protrusion  of  the  sac  bodily  into  or  through  the  micro- 
pyle may  be  regarded  as  only  a  more  extensive  development  of 
the  vermiform  micropylar  haustorium,  but  it  deserves  separate 
mention.  Torenia  is  the  oldest  and  most  conspicuous  illustra- 
tion of  this  phenomenon,  the  sac  passing  beyond  the  micropyle 
and  even  reaching  the  wall  of  the  ovary.  The  phenomenon 
also  occurs"  among  the  Rubiaceae,  the  sac  entering  the  micro- 
pyle in  Diodia  and  the  Galieae,  while  in  Vaillantia  the  mega- 
spore  mother-cell  passes  into  the  micropyle  and  divides  there. 

The  projection  of  the  synergid  as  an  haustorium  has  been 
observed  by  Billings  10°  in  Calendula  lusitanica,  in  which  the 
synergid  develops  into  the  micropyle  and  enlarges  greatly ;  and 
in  TrapeUa  (Oliver21),  large,  persistent  synergids  occur,  which 
are  evidently  haustorial.  Other  synergid  haustoria  have  been 
reported,  as  in  Lobelia,  but  they  prove  to  be  merely  haustoria 
from  the  sac,  containing  endosperm. 

The  antipodal  cells  are  often  very  prominently  associated 
with  the  haustorial  apparatus  for  obtaining  nutritive  supplies 
from  or  through  the  chalazal  region.  The  nutritive  function  of 
the  antipodals  seems  to  have  been  claimed  first  by  Wester- 
maier  23>  39  in  his  studies  of  the  prominent  antipodals  of  the 
Ranunculaceae.  This  was  confirmed  by  Osterwalder  60  in  his 
study  of  Aconitum  Napellus;  and  also  by  Mile.  Goldflus  61  in 
connection  with  the  Compositae.  The  latest  contribution  to  the 
subject  is  that  by  Ikeda,106  in  connection  with  Tricyrtis  hirta, 
who  claims  that  the  antipodals  in  that  species  are  nutritively 
active  from  the  full  maturation  of  the  sac  to  the  formation  of 
endosperm,  after  which  they  change  in  structure  and  gradually 
weaken ;  and  that  during  that  period  they  not  only  elaborate 
food  for  endosperm-formation,  but  also  for  the  growth  of  the 
egg-apparatus.  The  cutinization  of  the  integument  prevents 
the  passage  of  materials  except  by  way  of  the  chalaza,  and 
hence  much  of  the  nutrition  must  pass  through  the  antipodals. 
Ikeda  describes  and  figures  the  position  of  starch,  dextrine, 
and  cutinized  membranes  at  various  stages  in  the  development 
of  the  ovule  and  embryo  (Fig.  52).  From  this  point  of  view 
antipodals  are  of  two  general  types,  that  may  be  spoken  of  as 
the  passive  and  aggressive  types.  In  the  passive  type  the  antip- 
odals remain  active,  often  become  very  much  enlarged  (as 
among  Ranunculaceae),  or  even  form  a  mass  of  tissue  (as  in 


112 


MORPHOLOGY  OF  ANGIOSPERMS 


tSparganium),  but  they  are  not  associated  with  an  invasion  of 
the  chalazal  region,  and  simply  receive  material  from  it.  This 
type  is  characteristic  of  Monocotyledons  (except  Gramineae) 


Starch  (abundant}. 


(scanty). 


Dextrine. 


Cuticularized  membranes. 


FIG.  52. — Tricyrtis  hirta.  Various  stages  in  development  of  ovules,  embryo-sac,  and 
embryo,  showing  the  starch,  dextrine,  and  cutinized  membranes  at  different  periods, 
the  sequence  being  indicated  by  the  letters  A-G-.— After  IKEDA.IO« 

and  Archichlamydeae  (except  many  Amentif erae) .  In  the 
aggressive  type,  active  and  often  multiplying  antipodals  are 
associated  with  the  penetration  of  the  chalazal  region  by  the 


THE  FEMALE  GAMETOPHYTE  113 

antipodal  portion  of  the  sac.  This  type  is  characteristic  of 
Sympetalae,  perhaps  being  especially  prominent  among  the 
Kubiaceae  and  Compositae;  but  it  is  also  conspicuous  among 
the  Gramineae  and  Amentiferae.  Among  the  Amentiferae  it 
is  noteworthy  that  an  antipodal  haustorium  occupied  by  active 
antipodal  cells  and  a  special  vermiform  haustorium  occupied 
by  endosperm  cells  are  often  both  present. 

That  every  suspensor  is  an  haustorium  for  the  embryo 
seems  evident,  but  aside  from  this  general  fact  special  out- 
growths from  the  suspensor  are  developed  to  reach  a  wider 
range  of  nutritive  supplies.  The  case  of  certain  orchids  whose 
suspensors  develop  vermiform  haustoria  that  envelop  the  em- 
bryo, or  grow  through  the  micropyle  and  embed  themselves  in 
the  wall  of  the  ovary,  has  long  been  known;  and  it  has  been 
recently  found  that  among  certain  Rubiaceae  (Galieae)  the 
filamentous  suspensor  sends  out  conspicuous  lateral  processes 
or  branches  that  penetrate  the  endosperm  (Lloyd105). 

In  some  cases  a  complex  mechanism  for  nutrition  has  been 
described,  and  numerous  others  will  be  discovered  when  atten- 
tion is  given  to  the  subject.  The  case  of  Phlox  Drummondiij 
as  described  by  Billings,100  may  be  used  as  an  illustration.  The 
wall  of  the  ovary  adjacent  to  the  micropyle  develops  a  papilla 
of  special  structure  consisting  of  elongated  cells.  This  presses 
against  the  micropyle,  which  becomes  closed  and  resembles  con- 
ducting tissue.  A  papilla  of  small  cells  develops  from  the  adja- 
cent integument  in  contact  with  the  sac,  and  pressing  into  it  is 
put  in  connection  with  the  suspensor.  In  testing  this  mecha- 
nism for  starch,  Billings  found  starch  in  the  ordinary  tissue  of 
the  ovary  wall,  no  starch  in  the  wall-papilla,  and  abundant 
starch  again  in  the  integument  bordering  the  old  micropyle. 
This  seems  to  establish  a  definite  passage  of  nutritive  supplies 
from  the  ovary  wall,  through  a  series  of  specially  developed 
tissues,  to  the  suspensor. 

In  Stylidium  squamellosum  (Burns  85)  there  is  a  remarkable 
combination  of  nutritive  structures  (Fig.  50).  The  micropylar 
end  of  the  sac  enlarges  enormously  and  spreads  out  through  the 
thick  integument,  a  remarkable  nutritive  jacket  of  radially 
elongated  cells  invests  the  lower  part  of  the  sac,  and  a  distinct 
gland-like  nutritive  tissue  is  developed  in  the  chalaza  adjacent 
to  the  antipodal  end  of  the  sac. 


114  MORPHOLOGY  OF  ANGIOSPERMS 


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78.  CONRAD,  A.  H.     A  Contribution  to  the  Life-History  of  Quercus. 

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85.  BURNS,  G.  P.    Beitrage  zur  Kenntniss  der  Stylidiaceen.    Flora  87 : 

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THE  FEMALE  GAMETOPHYTE  119 

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93.  -      — .    Ueber  die  Pollenbildung  von  Zostera.    Meddel.  Stock- 

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96.  STRASBURGER,  E.    Einige  Bemerkungen  zu  der  Pollenbildung  bei 

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100.  BILLINGS,  F.  H.    Beitrage  zur  Kenntniss  der  Samenentwicklung. 

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104.  OLIVER,  F.  W.    On  a  Vascular  Sporangium  from  the  Stephanian 

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pis.  3-6.  1902. 

107.  GUIGNARD,  L.    La  double  fecondation  chez  les  Solanees.    Jour. 

Botanique  16:  145-167.  figs.  45.  1902. 

108.  STRASBURGER,  E.    Ein  Beitrag  zur  Kenntniss  von  Ceratophyllum 

submersum  und  phylogenetische  Erorterungen.  Jahrb.  Wiss. 
Bot.  37:  477-526.  pis.  9-11.  1902. 

109.  HALL,  J.  G.    An  Embryological  Study  of  Limnocharis  emargi- 

nata.    Bot.  Gazette  33:  214-219.  pi.  9.  1902. 

110.  OVERTON,  J.  B.    Parthenogenesis  in  Thalictrum  purpurascens. 

Bot.  Gazette  33 :  363-375.  pis.  12-13.  1902. 
9 


120  MORPHOLOGY  OF  ANGIOSPERMS 

111.  WEBB,  J.  E.     A  Morphological  Study  of  the  Flower  and  Embryo- 

of  Spiraea.     Bot  Gazette  33 :  451-460.  figs.  28.  1902.     For  cor- 
rection of  names  see  REHDER  in  Bot.  Gazette  34 :  246.  1902. 

112.  DUCAMP,  L.     Recherches  sur  1'embryogenie  des  Araliacees.    Ann. 

Sci.  Nat.  Bot.  VIII.  15:  311-402.  pis.  6-13.  1902. 

113.  MURBECK,  S.    Ueber  Anomalien  im  Baue  des  Nucellus  und  des 

Embryosackes  bei  parthenogenetischen  Arten  der  Gattung  Al- 
chemilla.    Lunds  Univ.  Arsskrift  38* :  no.  2.  pp.  10.  pi.  1.  1902. 

114.  JOHNSON,  D.  S.     On  the  Development  of  Certain  Piperaceae. 

Bot.  Gazette  34:  321-340.  pis.  9-10.  1902. 

115.  KARSTEN,  G.     Ueber  die  Entwicklung  der  weiblichen  Bliithen 

bei  einigen  Juglandaceen.    Flora  90:  316-333.  pi.  12.  1902. 

116.  ERNST,  A.     Chromosomenreduction,  Entwicklung  des  Embryo- 

sackes und  Befruchtung  bei  Paris  quadrifolia  L.  und  Trillium 
grandiflorum  Salisb.    Flora  91 :  1-46.  pis.  1-6.  1902. 

117.  ENDRISS,  W.    Monographic  von  Pilostyles  ingae  (Karst.)  (Pilo- 

styles  Ulei  Solms-Laub.).    Flora  91 :    209-236.  pi  20.  figs.  29. 
1902. 

118.  FRYE,  T.  C.    A  Morphological  Study  of  Certain  Asclepiadaceae. 

Bot.  Gazette  34:  389-413.  pis.  13-15.  1902. 

119.  .    The  Embryo-sac  of  Casuarina  stricta.    To  .be  published 

in  Bot.  Gazette  35 :  1903. 

120.  FERRARIS,  T.     Ricerche  embriologiche  sulle  Iridaceae.     I.  Em- 

briologia  del  G.  Romulea  Maratti.    Ann.  R.  Istit.  Bot.  Roma  9  * 
221-241.  pis.  6-7.  1902. 

121.  JUEL,  H.  O.     Zur  Entwicklungsgeschichte  des  Samens  von  Cyno- 

morium.     Beih.  Bot.  Centralbl.  13 :  194-202.  figs.  5.  1902. 

122.  SHIBATA,  K.    Experimentelle  Studien  liber  die  Entwickelung  des 

Endosperms   bei    Monotropa.     (Vorlaufige    Mitteilung.)     Bioh 
^Centralbl.  22:  705-714.  1902. 


CHAPTEE    VI 

THE   MALE   GAMETOPHYTE 

THE  reduced  number  of  chromosomes  appears  at  the  first 
mitosis  in  the  pollen  mother-cell,  which  is  therefore  the  first 
gametophytic  cell  (Fig.  53).  In  every  case,  so  far  as  known, 
two  divisions  occur  in  rapid  succession,  giving  rise  to  four 
microspores.  Strasburger 8  has  called  attention  to  the  two 
modes  of  division.  In  one  case,  most  frequent  among  Mono- 
cotyledons, a  wall  follows  the  first  nuclear  division,  dividing 
the  mother-cell  into  two  hemispherical  cells ;  the  second  nuclear 
division  is  also  followed  immediately  by  the  formation  of  a 
wall,  making  two  equal  cells  from  each  of  the  hemispheres  (Fig. 
54).  In  the  other  case,  more  characteristic  of  the  Dicotyledons, 
the  two  nuclear  divisions  occur  before  any  walls  are  formed, 
all  the  walls  being  then  formed  simultaneously  and  in  such  a 
way  that  each  of  the  four  cells  has  the  form  of  a  triangular 
pyramid  with  a  spherical  base — that  is,  each  cell  is  the  quadrant 
of  a  sphere  (Figs.  55,  56).  The  former  method  has  been  called 
successive,  the  latter  simultaneous  division.  The  two  modes 
are  not  sharply  characteristic  of  the  two  great  groups  of  Angio- 
sperms,  but  the  successive  method  is  dominant  among  Mono- 
cotyledons and  the  simultaneous  among  Dicotyledons.  In  any 
event  the  result  is  a  tetrad^  a  group  of  four  cells  each  of  which 
is  a  microspore.  In  successive  division  there  is  a  bilateral  ar- 
rangement of  the  microspores,  and  in  simultaneous  division  the 
arrangement  is  tetrahedral ;  but  both  arrangements  sometimes 
occur  in  the  same  sporangium. 

The  arrangement  of  the  tetrad  is  not  always  restricted  to 
these  two  methods  (Fig.  57).  Wille  15  has  described  varying 
arrangements  of  microspores  in  the  tetrads  of  species  of  Juncus 
and  Orchis  mascula]  and  in  TypJia  Schaffner  34  not  only  found 

121 


122 


MORPHOLOGY  OF  ANGIOSPERMS 


the  tetrads  indiscriminately  tetrahedral  or  bilateral,  but  fre- 
quently the  four  spores  are  in  a  row.  A  tetrad  consisting  of 
four  spores  in  a  row  has  also  been  found  by  Strasburger  54  and 


FIG.  53. — Lilium  Martagon.  A,  transverse  section  of  young  microsporangium,  showing 
two  nuclear  mitotic  figures  in  sporogenous  cells  and  one  in  a  hypodermal  cell ;  such 
figures  show  24  chromosomes,  the  sporophyte  number ;  x  200.  B,  chromosomes  of 
a  mitotic  figure  in  the  wall  of  a  microsporangium,  showing  24  chromosomes ;  x  600. 
(7,  pollen  mother-cell ;  polar  view  of  the  first  mitosis,  showing  12  chromosomes,  the 
gametophyte  number,  in  the  nuclear  plate;  the  segments  are  double,  one-half  of 
each  segment  will  pass  to  each  pole  ;  x  625.  /),  later  stage  in  first  mitosis  showing 
12  chromosomes,  each  chromosome  representing  one-half  of  one  of  the  12  segments 
shown  in  C\  x  625. — After  GUIGNARD." 

by  Frye  56  to  occur  regularly  in  Asclepias  and  allied  genera ;  by 
Rosenberg 57  in  Zostera ;  and  Neottia  nidus-avis  is  cited  by 
Goebel16  (p.  368). 

It  has  been  claimed  that  in  Zostera,  Cyperaceae,  Clematis, 
Helianthemum,  Epilobium,  Asclepias,  and  Lappa,  only  one 
microspore  is  formed  by  a  mother-cell.  In  every  case  except 


THE  MALE    GAMETOPHYTE 


123 


Zostera,  Cyperaceae,  and  Asclepias  the  claim  was  disproved 
long  ago ;  and  even  these  have  now  been  cleared  up,  so  that  no 
case  is  known  in  which  a  pollen  mother-cell  becomes  a  micro- 
spore  directly  without  the  tetrad  divisions.  It  does  not  seem 
improbable  that  such  a  case  may  exist,  for  cases  of  oogenesis 


D 


G  H 

FIG.  54.— Fritillaria  persica.  Sections  showing  the  two  nuclear  divisions  by  which  four 
raicrospores  are  formed  in  the  mother-cell  by  the  successive  (bilateral)  method; 
x  530.  A,  very  young  mother-cell;  B,  nucleus  in  synapsis;  <?,  12  chromosomes, 
one  of  them  rather  indistinct,  within  the  nucleus;  Z>,  mitotic  figure  of  the  first 
division  showing  the  short,  thick  chromosomes  characteristic  of  the  reduction 
division;  E,  later  stage  of  first  division,  showing  vertical  view  of  the  12  chromo- 
somes ;  F,  side  view  of  same  stage  showing  12  chromosomes  passing  to  the  upper 
pole,  only  10  for  the  lower  pole  being  in  sight ;  G,  formation  of  wall  between 
daughter  nuclei ;  Zf,  second  division ;  /,  formation  of  walls. — After  STKASBUKGER.I() 

like  that  of  Lilium  are  not  rare,  where  the  mother-cell  gives 
rise  directly  to  a  single  megaspore.  As  stated,  in  1886  Wille  15 
found  no  tetrad  in  Asclepias  syriaca;  and  in  1892  Chau- 
veaud  20  observed  the  reduction  division  of  the  pollen  mother- 


124 


MORPHOLOGY  OF  AXGIOSPERMS 


cells  of  Cynanchum,  but  seems  not  to  have  noted  the  formation 
of  a  tetrad;  but  the  tetrad,  consisting  of  a  row  of  four  micro- 
spores,  and  referred  to  above  as  discovered  by  Strasburger  and 
by  Frye  in  1901  in  a  number  of  species  of  Asdepias  and  in 
Cynanchum,  was  so  unusual  as  to  disguise  its  tetrad  nature,  and 


A  B  C 

TPiQ.tt.—PodophyllumpeUatum.  Mitosis  in  pollen  mother-cell.  A,  telophase  of  first 
division ;  £,  late  anaphase  of  second  division ;  (7,  telophase  of  second  division ;  the 
nuclei  of  the  four  microspores  are  formed,  but  the  cell  walls,  as  is  characteristic  of 
simultaneous  division,  have  not  yet  appeared. — After  MoxTiEE.29 

besides,  the  enlargement  and  consequent  readjustment  of  the 
spores  soon  break  up  the  row  (Fig.  58).  The  first  record  of 
the  occurrence  of  a  tetrad  in  Asdepias  seems  to  have  been  made 
by  Stevens  41  in  1898 ;  and  the  fourth  independent  discovery 
of  it  was  by  Gager  58  in  1902.  Elving,7  Wille,15  and  Stras- 
burger 12  showred  that  in  various  species  of  the  Cyperaceae  a 
tetrad  is  formed  although  only  one  microspore  becomes  func- 
tional, the  other  soon  disorganizing.  Juel  50  has  recently  made 
a  thorough  study  of  Car  ex  acuta  (Fig.  59).  He  finds  that  the 
two  characteristic  nuclear  divisions  take  place,  and  that  a 
cell-plate  is  formed  at  each  division.  The  cell-plates  are  soon 
resorbed,  however,  so  that  the  four  nuclei  lie  free  within  the 
wall  of  the  mother-cell.  Three  of  the  nuclei  then  disintegrate, 
while  the  fourth  becomes  the  nucleus  of  the  single  functional 
microspore;  and  the  wall  of  the  mother-cell,  inclosing  the  four 
nuclei,  becomes  the  wall  of  the  microspore.  In  Zostera  marina 
Rosenberg  57  has  described  the  tetrad  division  of  the  remarkably 
elongated  mother-cell  (Fig.  11).  The  divisions  are  longitudinal 
and  in  parallel  planes,  resulting  in  four  remarkable  filiform 


THE  MALE   GAMETOPHYTE 


125 


microspores  lying  side  by  side,  and  measuring  3  by  2,000  p 
when  mature.  That  this  is  a  tetrad  is  evident  from  the  rapid 
succession  of  the  divisions,  the  reduction  of  chromosomes,  and 
the  formation  of  four  spores  from  a  mother-cell. 

In  some  cases  a  mother-cell  may  give  rise  to  less  than  four 
microspores,  or  may  produce  more  than  the  normal  number 
(Fig.  60).  In  1886  Wille  15  summarized  the  work  of  previous 
investigators,  notably  of  Hofmeister,  Tangl,  Wimmel,  and 
Tschistiakoff,  and  added  the  results  of  his  own  investigations. 
The  following  lists  are  made 
up  largely  of  forms  investi- 
gated by  Wille  himself: 

Two  microspores  from 
a  mother-cell  are  occasion- 
ally found  in  Convallaria 
multiflora,  Asparagus  offi- 
cinalis,  Aconitum  Napellus, 
Euphorbia  Lathyrus,  Be- 
gonia sp.,  Saxifraga  caespi- 
tosa,  Azalea  indica,  and 
Syringa  vulgaris. 

Three  microspores  were 
found  in  Begonia  sp.,  Sa.i't- 
fraga  caespitosa,  Azalea  in- 
dica',  and  Lonicera  coerulea. 

Five  microspores  were 
found  in  Funkia  ovata,  Fi- 
ta  ria  ra  n  u  n  c  u  lo  ides,  Ste  l- 
/c  /•  ia  qla  u  ca,  Scleran  tli  us 
annuus,  Primus  Cerasus, 
Eumex  Patientia,  Azalea 
indica,  Lonicera  coerulea, 
Syringa  persica,  and  Sym- 
pliylum  officinal e. 

Six  microspores  were  found  in  Hemerocallis  fulva,  Ficaria 
ranunculoides,  Elaline  hexandra,  Cornus  sanguinea,  Lonicera 
coerulea,  and  Fuchsia  sp. 

Seven  microspores  were  counted  with  certainty  in  Fuchsia 
sp.  and  fourteen  are  reported  rather  doubtfully;  eight  is  given 
for  Azalea  indica,  and  eight  to  twelve  for  Lonicera  coerulea, 


FIG.  56. — Scrophularia  nodosa.  Section  of  mi- 
crosporangium  showing  appearance  of  spores 
formed  by  the  simultaneous  method;  the 
inner  tapetum  of  microsporangium  consists 
of  greatly  elongated  cells  which  are  very 
glandular  in  appearance,  x  275. 


126 


MORPHOLOGY  OF  ANGIOSPERMS 


O 


B 


but  it  was  not  absolutely  certain  that  in  case  of  the  higher  num- 
bers all  the  microspores  came  from  the  same  mother-cell.  In 
Hemerocallis  fulva  Strasburger  10  has  counted  nine  microspores 
f  rom  a  single  mother-cell ;  and  later  Juel  33  and  Fullmer  44  re- 
ported six  to  eight  in  the  same  species.  More  recently  Miss 
Lyon  40  has  found  five  or  six  microspores  of  equal  size  produced 
by  a  single  mother-cell  of  Euphorbia  corollata. 

According  to  Wille,  two  microspores  result  from  a  failure 
of  the  mother-cell  to  undergo  the  second  division.  When  three 
are  formed,  the  first  division  is  unequal,  and  only  the  larger 

cell  divides.  Five  or 
more  microspores  are 
formed  by  subsequent 
division  of  one  or  more 
members  of  the  tetrad. 

Strasburger,10  Juel,33 
and  Fullmer,44  in  their 
study  of  Hemerocallis 
fulva  found  an  explana- 
tion of  the  irregular 
numbers.  Strasburger 
found  that  chromosomes 
which  fail  to  pass  to 
either  pole  at  the  first 
mitosis  give  rise  to  small 
microspores.  Juel  in  his 
more  recent  study  con- 
firms Strasburger,  and 
finds  that  even  single 
chromosomes  which  be- 
come separated  may  divide  and  give  rise  to  nuclei  and  organize 
cells.  Fullmer  attributes  the  supernumerary  microspores  to  the 
division  of  one  or  more  members  of  the  tetrad. 

Perhaps  no  phase  of  plant  cytology  has  received  so  much 
attention  as  the  nuclear  divisions  in  the  pollen  mother-cell.  It 
is  an  interesting  fact  that  the  cytological  characters  of  these  two- 
mitoses  agree  minutely  with  those  in  the  megaspore  mother- 
cell.  The  pollen  mother-cell  can  be  positively  identified  by  the 
appearance  of  the  synapsis  stage  (Fig.  54,  J5),  even  before  any 
rounding  off  or  separation  takes  place.  While  yet  in  the  spirem 


Fio.  57. — Variation  in  the  arrangement  of  the  spores 
of  a  tetrad.  A-C,  Orchis  mascula,  x  380;  after 
WILLE."  D-E,  Typha  latifolia,  x  400 ;  after 

SCHAFFNER.34 


FIG.  58.— Development  of  male  gametophyte  in  Asdepias.  A-B,  A.  Comuti;  C-E,  A. 
tuberosa.  A,  section  of  young  microsporangiurn  showing  archesporial  cells;  Ji, 
portion  of  the  single  layer  of  elongated  mother-cells;  C\  later  stage  showing  two 
mother-cells,  the  lower  one  dividing  and  showing  10  chromosomes,  the  gametophyte 
number;  Z>,  second  division  of  mother-cell,  by  which  the  row  of  four  microspores  is 
formed ;  E,  microspore  showing  tube  nucleus  (t)  and  generative  nucleus  (<?).  A, 
x  200 ;  B-E,  x  800.— After  FRYE.<* 

127 


128 


MORPHOLOGY  OF  ANGIOSPERMS 


stage  the  chromatin  thread  splits  longitudinally  throughout  its 
entire  length  (Fig.  61,  A9  B).  The  double  thread  then  seg- 
ments transversely  into  the  number  of  chromosomes  characteris- 


.  59. — Development  of  microspores  in  Heleocharis palustris  and  Carex  acuta.  A-B, 
Heleocharis,  showing  the  single  functional  microspore  and  three  disorganizing  micro- 
spores,  x  380 ;  after  STRASBURGER.18  C-I,  Carex :  C,  mother-cell ;  Z>,  second  division ; 
F,  four  nuclei,  only  three  of  which  are  shown  within  the  mother-cell  (E  and  F 
should  be  reversed) ;  E,  later  stage  than  F\  the  nucleus  of  the  functional  micro- 
spores  is  preparing  for  division;  £,  tube  nucleus,  generative  cell,  and  lower  down 
the  nuclei  of  the  three  non-functional  microspores ;  H,  nearly  ripe  pollen  grain ;  7, 
irregular  case  in  which  the  nuclei  of  the  three  non-functional  microspores  have 
divided;  x  900.— After  JUEL.M 

tic  of  the  gametophyte  of  a  given  species,  each  chromosome  thus 
being  made  up  of  two  pieces  (Fig.  53,  (7).  According  to  several 
investigators,  a  second  longitudinal  splitting  of  the  chromo- 
somes may  be  seen  during  the  anaphase  of  the  first  mitosis,  so 
that  the  two  mitoses  merely  distribute  the  reduced  number  of 
chromosomes  which  appear  just  after  the  segmentation  of  the 
spirem.  In  the  subsequent  mitoses  the  spirem  segments  into 
chromosomes  which  afterward  split  longitudinally  as  in  vege- 
tative cells. 

It  is  in  the  divisions  of  the  pollen  mother-cell  that  the 
problem  of  the  reduction  of  chromosomes  has  been  studied  most 
thoroughly;  but  while  it  is  agreed  that  the  reduced  number 
appears  at  the  first  mitosis,  there  is  still  some  difference  of 


THE  MALE  OAMETOPHYTE 


129 


opinion  as  to  whether  a  qualitative  division  occurs.    At  present 
the  weight  of  evidence  is  against  such  a  division. 

According  to  nearly  all  recent  observers  (Belajeff,24  Stras- 
burger,25  Mottier,26  Lawson,35  Miss  Byxbee  52)  the  spindle  in 
the  first  mitosis  originates  as  a  multipolar  structure,  which 


FIG.  60. — Microspore  mother-cells  producing  more  or  less  than  four  microspores.  A-B, 
Hemerocallis  fulva,  with  five  and  eight  microspores  in  process  of  formation ; 
A  x  1000;  B  x  625;  after  JuEL.33  <?,  Euphorbia  corollata,  with  five  microspores 
of  equal  size  within  mother-cell ;  x  625 ;  after  LYON.40  D,  Begonia  sp.,  with  three 
niicrospores  from  a  mother-cell ;  x  400.  E,  Ficaria  ranunculoides,  with  six  micro- 
spores,  x  400.  F,  Azalea  indica,  with  six  microspores,  three  having  come  from  the 
division  of  one  of  the  spores  of  the  tetrad,  x  400.  D-E,  after  WILLED 

gradually  becomes  bipolar  (Figs.  61,  61<z).  In  a  few  cases  mul- 
tipolar spindles  have  been  described  for  the  second  mitosis.  In 
vegetative  cells  the  spindle  first  appears  as  a  pair  of  dome- 
shaped  prominences  or  caps.  Transitions  between  the  two 
modes  are  not  lacking. 


130 


MORPHOLOGY   OP  ANGIOSPERMS 


The  number  of  chromosomes  observed  in  connection  with 
the  reduction  division  have  been  noted  in  the  preceding  chap- 
ter (p.  81). 


FIG.  61. — First  division  of  pollen  mother-cell,  showing  formation  of  the  bipolar  from  the 
multipolar  spindle.  A,  £,  E,  F,  Lilium  Martdgon ;  <?-Z>,  L.  candidum.  A,  double 
row  of  chromatin  granules  upon  the  linin  thread  ;  B,  later  stage  in  which  the  entire 
thread  has  split  longitudinally  ;  (7,  formation  of  a  weft  of  fibers  about  the  nucleus ; 
Z>,  multipolar  spindle ;  E,  bipolar  spindle ;  F,  telophase  of  first  division  showing- 
that  the  division  is  of  the  successive  type. — After  MoxTiER.26 


THE   MALE  GAMETOPHYTE  131 

After  the  two  divisions,  each  of  the  four  young  microspores 
becomes  invested  by  a  delicate  wall  which  is  independent  of  the 
common  wall  of  the  mother-cell.  This  wall  soon  becomes  differ- 
entiated into  two  layers,  the  inner  one  (intine)  consisting  of 
pure  cellulose  and  later  developing  the  pollen-tube. 

The  outer  layer  (exine)  is  cutinized,  and  especially  among 
Dicotyledons  becomes  variously  sculptured,  often  being  covered 
with  ridges,  wrarts,  spines,  etc.,  as  fully  described  by  Schacht  2 
and  Luerssen.5  For  the  most  part,  there  are  thin  spots  in  the 
exine  for  the  exit  of  pollen-tubes.  It  is  interesting  to  note  that 
only  a  single  point  of  exit  occurs  in  the  microspores  of  most 
Monocotyledons  and  of  a  few  Dicotyledons ;  while  in  most  Di- 
cotyledons there  are  from  two  to  many  such  points  of  exit. 
Goebel 16  (p.  367)  has  given  the  following 
illustrations  from  Schacht  2 :  two  points  of 
exit  in  Ficus,  Justicia,  etc. ;  three  in  Cupu- 
liferae,  Proteaceae,  Geraniaceae,  Onagra- 
ceae,  Boraginaceae,  and  Compositae;  four 
to  six  in  Alnus,  Carpinus,  Astrapaea,  and 
Impatiens;  many  in  Alsineae,  Malvaceae, 
Convolvulaceae,  etc.  Barnes 13  records 

,  ,  ,  .  ,  .  j.  ..—- 

three  to  twelve  thin  spots  in  the  exine  of  dum,  Muitipoiarspin- 
Campanula,  and  Coulter37  finds  fifteen  to  die  at  first  division 
thirty  such  areas  in  that  of  Ranunculus.  of  pollen  mother-cell ; 

.       ,  x  400. —  After  BELA- 

ln  certain  cases  a  much  more  specialized       JEFF." 
method  for  the  exit  of  the  pollen-tube  is 
provided,  as  among  the  Cucurbitaceae  and  in  Passiflora,  in 
which  roundish,  lid-like,  and  often  embossed  pieces  of  the  exine 
become  detached;  and  in  Thunbergia,  in  which  the  layer  of 
exine  splits  into  exfoliating  spiral  bands.    Among  those  aquatics 
that  pollinate  under  water,  as  well  as  in  the  pollinia-bearing 
forms,  the  .exine  is  said  to  be  lacking.     The  origin  and  devel- 
opment of  the  walls  of  spores  is  a  problem  that  needs  further 
investigation. 

For  the  most  part,  the  microspores  become  entirely  free 
from  one  another  at  maturity,  forming  a  pulverulent  mass,  but 
there  are  instances  of  microspores  failing  to  become  dissociated, 
giving  rise  to  the  so-called  "  compound  grains  "  (Figs.  13,  57). 
In  the  simplest  cases  the  four  spores  of  a  tetrad  cling  together, 
as  in  Typha,  certain  orchids  (as  Neottia),  Anona,  Fourcroya, 


132  MORPHOLOGY  OF  ANGIOSPERMS 

and  Rhododendron;  in  other  cases  the  whole  product  of  a 
primary  sporogenous  cell,  ranging  from  eight  to  sixty-four 
microspores,  clings  in  a  mass,  as  the  massulae  of  certain  orchids 
(Ophrydeae)  and  the  groups  of  pollen-grains  found  among  the 
Mimoseae;  and  in  the  most  extreme  cases,  the  whole  product 
of  a  sporangium  forms  a  single  mass,  the  pollinium,  character- 
istic of  certain  Orchids  and  of  the  Asclepiadaceae.  It  is  of 
interest  to  note  that  all  of  these  conditions  occur  among  Or- 
chidaceae,  from  isolated  microspores  (Cypripedium)  to  the  com- 
pletely organized  pollinium.  Such  variations  and  others  have 
been  described  in  detail  by  Reichenbach,1  Hofmeister,3  Rosa- 
noff,4  Corry,11  and  others. 

The  older  botanists  were  not  able  to  recognize  the  structures 
developed  within  the  mature  pollen-grain,  whose  contents  they 
called  "  fovilla,"  regarding  it  as  a  fertilizing  substance  rich  in 
food  material.  In  1878  Strasburger  6  discovered  that  struc- 
tures are  developed  in  the  microspores  of  Angiosperms  com- 
parable to  those  already  known  in  Gymnosperms,  and  this  was- 
confirmed  by  Elfving.7 

The  germination  of  the  microspore  begins  with  the  division 
of  its  nucleus,  and  this  always  occurs  before  dehiscence,  some- 
times long  before,  the  two  daughter  nuclei  having  been  found 
even  in  midwinter,  as  in  Alnus  and  Corylus  (Chamberlain38) 
(Fig.  8).  When  first  formed,  the  daughter  nuclei  are  usually 
alike  in  size  and  form,  but  in  most  cases  the  tube  nucleus  soon 
becomes  much  larger,  the  differentiation  sometimes  beginning^ 
as  in  Cypripedium,  before  the  mitosis  is  fully  completed  (Fig. 
62).  In  any  case,  the  nuclei  soon  become  differentiated,  the 
tube-nucleus  having  a  large  nucleolus  and  a  rather  scanty  chro- 
matin  network;  while  the  generative  nucleus  is  smaller,  has  a 
smaller  nucleolus  or  none  at  all,  and  its  chrbmatin  is  denser 
and  less  irregular.  The  nuclei  also  differ  in  their  reaction  to 
stains,  a  combination  like  cyanin  and  erythrosin  staining  the 
tube-nucleus  red  and  the  generative  nucleus  blue. 

At  first  Strasburger 6  thought  that  the  tube-nucleus  was 
concerned  not  merely  in  developing  the  pollen-tube,  but  also  in 
fertilizing  the  egg,  and  hence  named  it  the  "  generative  nu- 
cleus." The  other  nucleus,  although  seen  to  enter  the  tube  and 
even  divide,  was  thought  to  take  no  part  in  the  processes  con- 
nected with  fertilization,  and  was  called  the  "  vegetative  "  or 


THE  MALE  GAMETOPHYTE  133 

"  prothallial "  nucleus.  This  older  view  is  the  one  given  in 
Goebel's  Outlines  of  Classification  and  Special  Morphology.  In 
1884  Strasburger  12  recognized  the  real  nature  of  the  two  nuclei 
and  interchanged  the  names,  applying  them  as  they  have  been 
used  ever  since.  We  have  substituted  the  name  "  tube-nucleus  "" 
for  "  vegetative  nucleus,"  not  only  because  the  development  of 
the  tube  is  its  most  conspicuous  function,  but  also  because  it  is 


mfw  S  ~^J     ,^r 

%!' 

^  .,  ~  n 


J*     l£ 
f      *5 

e  / 

*  '.  e  .*% 

SL 


FIG.  62. —  Cypripedium  spectabile.  Section  of  microsporangium,  showing  microspores  in 
various  stages  of  division  into  tube  and  generative  nuclei ;  although  the  divisions- 
are  nearly  simultaneous  throughout  the  microsporangium,  it  will  he  seen  that  in 
some  cases  the  nuclei  are  in  the  spirem  stage,  while  in  others  the  tube  and  genera- 
tive nuclei  are  easily  distinguished ;  x  300. 

not  the  morphological  equivalent  of  the  vegetative  or  prothallial 
cells  of  the  Gymnosperms  and  heterosporous  Pteridophytes. 

A  generative  cell  is  formed  by  the  more  or  less  distinct  or- 
ganization of  the  cytoplasm  about  the  generative  nucleus.  This 
cell  usually  lies  free  in  the  body  of  the  spore,  but  is  often  cut 
off  by  a  distinct  wall,  as  in  Typha,  (Schaffner  31),  Sparganium 
(Campbell43),  Xaias  (Campbell29),  Convallaria  (Wiegand45), 
Neottia  (Guignard 9),  Populus  (Chamberlain30),  Asclepias 


134 


MORPHOLOGY  OF  ANGIOSPERMS 


(Frye  56);  and  Barcodes  (Oliver18).  Both  methods  are  often 
found  in  the  same  species  and  even  in  the  same  anther,  as  in 
Lilium  (Fig.  63). 

The  free  generative  cell  finally  assumes  a  variety  of  forms, 
the  most  common  being  lenticular,  the  cytoplasm  massing  chiefly 


FIG.  63. — Male  gametophyte  at  time  of  shedding.  JB,  C,  Lilium  auratum ;  the  others 
L.  tigrinum ;  x  500.  A,  generative  cell  against  side  of  microspore  ;  £,  generative 
cell  in  body  of  microspore ;  the  two  male  nuclei  already  formed ;  (7,  three  male 
nuclei  within  generative  cell,  an  unusual  case ;  D,  two  male  nuclei,  differing  in  size, 
within  generative  cell ;  E,  tube-nucleus  divided,  giving  rise  to  six  nuclei ;  F,  an 
unusual  case,  showing  tube-nucleus,  two  generative  cells  (g),  and  a  " prothallial" 
cell  (pr). — After  CHAMBERLAIN.33 

at  two  opposite  poles  of  the  nucleus.  In  some  cases  «a  spherical 
form  is  maintained,  as  in  Acer  (Mottier  22)  ;  in  others  the  len- 
ticular form  passes  into  the  vermiform,  becoming  elongated  and 


THE  MALE  GAMETOPHYTE  135 

even  coiled  or  twisted,  as  in  Tradescantia  (Coulter  and 
Rose  14)  ;  or  the  cytpplasm  of  the  spindle-shaped  generative  cell 
may  taper  into  elongated  whip-like  filaments  that  more  or  less 
encircle  the  tube-nucleus,  as  in  Eichhornia  (Smith39).  In 
Erythronium  Schaffner  55  found  that  the  generative  nucleus  is 
larger  than  the  tube  nucleus  and  is  surrounded  by  a  densely 
staining  amoeboid-form  mass  of  cytoplasm.  It  is  altogether 
probable  that  the  size  and  form  of  free  generative  cells  varies 
with  age  and  external  conditions,  so  that  they  may  be  relatively 
large  or  small ;  or  spherical,  lenticular,  spindle-shaped,  or  ver- 
miform in  the  same  species.  It  is  very  common  to  find  them  at 
first  spherical  and  later  lenticular,  as  has  been  frequently  ob- 
served in  Lilium. 

In  Lilium  iigrinum  Chamberlain  32  often  found  a  small  cell 
cut  off  by  the  microspore  before  the  appearance  of  the  tube  and 
generative  nuclei,  and  the  same  cell  was  noted  after  the  division 
of  the  generative  nucleus  (Fig.  63).  A  similar  cell  was  found 
by  Smith  39  in  Eichhornia  crassipes  and  by  Campbell  43  in  Spar- 
ganium  simplex.  It  is  suggestive  of  a  true  vegetative  or  pro- 
thallial  cell,  two  of  which  so  commonly  occur  among  the  Gym- 
nosperms;  but  the  phenomenon  is  too  unique  as  yet  among 
Angiosperms  to  deserve  more  than  a  mention. 

The  tube-nucleus  usually  increases  much  in  size,  and  under 
•certain  conditions  has  been  found  to  fragment,  as  in  Lilium,  in 
which  Chamberlain  32  found  four  and  in  one  case  eight  tube- 
nuclei  :  in  Eichhornia,  in  which  Smith  39  found  two  tube-nuclei 
in  half  the  pollen-grains  examined ;  in  Hemerocallis,  in  which 
Fullmer  44  reports  the  frequent  occurrence  of  two  to  six  tube- 
nuclei  ;  and  in  Asclepias,  in  which  Frye  56  observed  a  fragment- 
ing nucleus.  This  phenomenon  is  doubtless  not  uncommon  in 
certain  conditions  of  nutrition. 

The  generative  nucleus  or  cell  may  divide  in  the  pollen- 
grain,  even  long  before  dehiscence,  as  in  8agittaria  (Schaff- 
ner  31 )  ;  or  the  generative  cell  may  pass  into  the  tube  before 
•division,  sometimes  not  dividing  until  immediately  before  fer- 
tilization. The  time  of  this  division  seems  to  hold  no  relation 
to  the  great  plant  groups,  and  may  be  variable  in  the  same  genus 
or  even  species.  For  example,  in  Lilium  tigrinum  it  often 
takes  place  in  the  grain,  but  in  L.  philadelphicum  rarely  so; 
and  in  this  last  species  it  may  occur  either  in  the  grain  or  at 
10 


136  MORPHOLOGY  OF  ANGIOSPERMS 

any  time  in  the  tube  up  to  its  completed  growth.  The  variable 
relation  of  the  time  of  this  division  to  the  great  groups  may  be 
illustrated  by  the  following  record : 

Among  Monocotyledons  the  generative  nucleus  divides  in 
the  pollen-grain  in  Potamogeton  (Wiegand  45),  Alisma  (Schaff- 
ner28),  Sagittaria  (Sehaffner 31),  A  vena  (Cannon46),  Triti- 
cum  and  other  grasses  (Golinski  21),  Lemna  (Caldwell  42),  and 
Lilium  (Chamberlain32);  and  in  the  pollen- tube  in  Symplo- 
carpus  (Duggar47),  Tradescantia  (Coulter  and  Rose  14),  Eich- 
Jiornia  (Smith39),  Lilium  (Chamberlain32),  Convallaria 
(Weigand45),  Erythronium  (Schaffner55),  and  the  Orchids 
(Guignard  9).  In  examining  this  record  it  might  be  concluded 
that  the  early  division  of  the  generative  cell  within  the  pollen- 
grain  is  a  more  primitive  character  in  general  than  the  later 
division  in  the  pollen-tube.  Even  if  this  should  prove  to  be 
true  for  the  Monocotyledons,  it  can  hardly  be  claimed  for  the 
Dicotyledons,  as  the  following  record  shows: 

Among  Dicotyledons  the  generative  nucleus  or  cell  divider 
in  the  pollen-grain  in  Rhopalocnemis  (Lotsy51),  Pa-paver, 
Hesperis,  Archangelica,  and  Mertensia  (all  by  Strasburger12), 
Nicotiana  Tabacum  (Guignard59),  Sambucus  (Halsted 17), 
and  Silphium  (Merrell48)  ;  and  in  the  pollen-tube  in  Pepero- 
mia  (Johnson49),  Salix  (Chamberlain30),  Ranunculus  (Coul- 
ter37), Lathyrus  (Strasburger12),  Euphorbia  (Miss  Lyon  40), 
Staphylea  (Strasburger12),  Acer  (Mottier22),  Vinca,  Nemo- 
phila,  Digitalis,  and  Torenia  (all  by  Strasburger12),  Campa- 
nula (Barnes13),  and  Datura  laevis  (Guignard59).  It  is 
evident  that  the  two  conditions  are  found  among  Dicotyledons 
in  both  primitive  and  high  groups,  and  even  in  the  same  family 
(as  Solanaceae),  and  that  neither  one  has  any  claim  to  be 
regarded  as  an  essentially  primitive  character. 

The  male  nuclei,  formed  by  the  division  of  a  generative  nu- 
cleus, are  possibly  always  associated  with  cytoplasm  in  such 
a  way  that  definite  male  cells  are  organized.  The  nucleus  is 
often  the  only  conspicuous  feature,  and  in  every  case  it  finally 
constitutes  the  bulk  of  the  male  cell.  In  fact,  in  most  of  the 
plants  studied  only  the  male  nucleus  has  been  demonstrated  in 
the  pollen-tube  and  embryo-sac.  In  the  following  citations 
"  male  nucleus  "  and  "  male  cell  "  are  used  to  indicate  whether 
cytoplasm  was  demonstrated  or  not.  Various  forms  of  male 


THE   MALE  GAMETOPHYTE 


137 


cells  and  nuclei  have  been  described,  but  it  is  evident  that  the 
form  as  well  as  the  size  may  change  decidedly  in  the  course  of 
its  history.  For  example,  Schaffner  31  notes  that  the  male  nuclei 
in  Sag  iff  aria  are  at  first  spherical,  but  after  pollination  become 
bean-shape  or  spindle-shape.  In  Silphium  Merrell  48  observed 
the  originally  spherical  male  nuclei  become  much  elongated,  more 
or  less  curved,  and  even  spirally  twisted  while  still  within  the 
pollen-grain  (Fig.  6-i)  ;  and  in  Triticum  and  other  grasses  Go- 
linski  21  implies  the  same  changes  in 
form  in  describing  the  occurrence  of 
male  nuclei  within  the  pollen-grain 

•  not  unlike  the  antherozoids  of  a 
fern  or  of  Cliara"  It  has  been  re- 
peatedly observed  that  the  spherical 
nuclei  of  the  oblong  or  lenticular 
male  cells  of  Lilium  increase  in  size 
and  become  vermiform  and  variously 
curved  and  coiled  after  discharge 
from  the  pollen-tube,  and  the  same 
phenomenon  was  observed  by  Miss 
Thomas  53  in  Caltha. 

It  seems  to  be  generally  true  that 
the  male  cells  when  formed  free  in 
the  body  of  the  grain  are  at  first 
spherical,  but  soon  become  oblong  or  FIG. 
lenticular.  In  a  forthcoming  paper 
by  Koernicke  it  will  be  shown  that  in 
Lilium  only  male  nuclei  are  found  in 
the  pollen-tube;  at  least  there  are  no 
male  cells  as  ordinarily  figured.  This 
claim  is  of  special  interest,  since  in 
Lilium  male  cells  are  clearly  organized  in  the  pollen-grain. 
The  increase  in  size  and  change  of  form  so  often  described  as 
taking  place  in  the  tube  or  sac  are  probably  phenomena  of  the 
male  nucleus  rather  than  of  the  male  cell.  There  are  well- 
known  cases,  however,  in  which  the  spherical  or  oblong  form 
persists  throughout  the  history  of  the  nucleus.  For  example,  in 
Peperomia  (Johnson49)  the  male  nucleus  is  spherical  even  in 
contact  with  the  egg,  and  the  same  is  true  of  several  other  forms 
recently  investigated  in  connection  with  double  fertilization. 


A,  microspore  of  SilpM- 
wm  integrifolium,  showing  tube- 
nucleus  and  two  male  nuclei. 
£,  later  stage  in  S..  terebinthina- 
ceum,  showingi  the  two  male 
cells.  <7,  single  male  cell  of  6T. 
integrifolium,  showing  spiral 
form. — After 


138  MORPHOLOGY  OF  ANGIOSPERMS 

There  is  also  indication  that  the. two  male  nuclei  may  be- 
come differentiated  in  form,  as  in  the  case  of  Alisma,  in  which 
Schaffner  28  found  the  upper  male  nucleus  in  the  pollen-tube 
elongated  or  spindle-shaped,  and  the  lower  one  spherical.  It 
is  also  probable  that  in  cases  of  double  fertilization  the  two 
male  nuclei  often  assume  different  forms  in  the  embryo-sac. 
Four  male  nuclei  have  been  reported  by  Strasburger  12  as  some- 
times occurring  in  Camassia  Fraseri,  and  Chamberlain  32  has 
observed  three  nuclei  within  a  single  male  cell  in  Lilium  aura- 
turn  (Fig.  63,  (7).  This  recalls  the  spermatogenesis  of  Gymno- 
sperms, in  which  the  generative  cell  gives  rise  to  a  stalk  cell 
and  two  male  cells,  but  it  may  have  no  further  significance 
than  that  any  active  cell  may  be  induced  to  divide  by  favorable 
conditions. 

The  morphology  of  the  structures  included  in  the  male 
gametophyte  of  Angiosperms  is  obscure.  In  1884  Stras- 
burger 12  suggested  that  only  an  antheridium  is  developed 
within  the  pollen-grain,  the  vegetative  or  prothallial  tissue,  rep- 
resented in  many  Gymnosperms,  having  been  entirely  sup- 
pressed. The  same  view  has  been  developed  in  several  papers 
from  this  laboratory,  and  in  1898  Belajeff 36  reiterated  it  in 
a  discussion  including  both  Gymnosperms  and  Angiosperms. 
According  to  this  view,  the  larger  tube-cell  is  the  antheridium 
wall  that  develops  a  tubular  outgrowth,  used  at  least  in  Angio- 
sperms as  the  carrier  of  the  male  nuclei,  while  the  generative 
cell  and  its  product  is  the  spermatogenous  part  of  the  antherid- 
ium. It  is  not  exact  to  say  that  according  to  this  view  the 
whole  pollen-grain  is  an  antheridium,  but  that  in  its  germina- 
tion the  pollen-grain  develops  only  an  antheridium. 

Another  view,  which  seems  to  be  the  only  alternative,  is 
that  while  only  an  antheridium  is  present  its  sole  representative 
is  the  generative  cell,  the  tube-cell  not  being  any  more  a  part 
of  the  gametophyte  than  is  the  embryo-sac.  The  divergence 
between  the  two  views,  therefore,  has  to  do  only  with  the  nature 
of  the  tube-cell.  In  any  event,  it  is  important  to  note,  as  contra- 
dicting a  very  common  statement,  that  the  pollen-tube  is  not  the 
male  gametophyte. 

The  development  of  the  pollen-tube  and  the  passage  of  the 
male  nuclei  to  the  embryo-sac  are  so  directly  connected  with 
fertilization  that  they  will  be  considered  in  the  next  chapter. 


THE  MALE  GAMETOPHYTE  139 


LITERATURE    CITED 

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et  de  Orchideis  in  artem  ac  systema  regigendis.     Leipzig.  1852. 

2.  SCHACHT,  H.     Ueber  den  Bau  einiger  Pollenkorner.    Jahrb.  Wiss. 

Bot.  2 :  107-168.  pis.  1^18.  1860. 

3.  HOFMEISTER,  W.     Neue   Beitrage   zur    Kenntniss    der  Embryo- 

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Wiss.  6:  533-672.  pis.  1-27.  1859. 

4.  ROSANOFF,  S.    Zur  Kenntniss  des  Baues  und  der  Entwicklungsge- 

schichte  des  Pollens  der  Mimoseae.    Jahrb.  Wiss.  Bot.  4:  441- 
450.  pis.  31-32.  1865. 

5.  LUERSSEN,  C.     Zur  Controverse  iiber  die  Einzelligkeit  oder  Mehr- 

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Jenaisch.  Zeitsch.  Naturwiss.  13 :  1-28.  1879 ;  Quart.  Jour.  Micr. 
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8.  STRASBURGER,   E.    Zellbildung  und  Zelltheilung.    Ed.  3.    Jena. 

1880. 

9.  GUIGNARD,  L.     Recherches  sur  le  developpement  de  1'anthere  et 

du  pollen  des  Orchidees.     Ann.  Sci.  Nat.  Bot.  VI.  14:  26-45.  pi. 
2.  1882. 

10.  STRASBURGER,  E.    Ueber  den  Theilungsvorgang  der  Zellkerne  und 

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etc.,  in  Asclepias  Cornuti.      Trans.  Linn.   Soc.    Bot.    London 
2:  173-207.  pis.  24-26.  1884. 

12.  STRASBURGER,  E.    Neue  Untersuchungen  iiber  den  Befruchtungs- 

vorgang  bei  den  Phanerogamen.     Jena.  1884. 

13.  BARNES,  C.  R.    The  Process  of  Fertilization  in  Campanula  amer- 

icana.    Bot.  Gazette  10 :  349-354.  pi.  10.  1885. 

14.  COULTER,  J.  M.,  and  ROSE,  J.  N.    The  Pollen  Spore  of  Tradescantia 

virgin  ica.    Bot.  Gazette  11:  10-14.  pi.  1.  1886. 

15.  WILLE,  N.    Ueber  die  Entwickelungsgeschichte  der  Pollenkorner 

der  Angiospermen  und  das  Wachsthum  der  Membranen  durch 
Intussusception.     Christiania.  1886. 

16.  GOEBEL,  C.     Outlines  of  Classification  and  Special  Morphology. 

English  translation.  1887. 

17.  HALSTED,  B.  D.    Three  Nuclei  in  Pollen  Grains.    Bot.  Gazette  12: 

285-288.  pi.  16.  1887. 

18.  OLIVER,  F.  W.    On  Sarcodes  sanguinea.    Annals  of  Botany  4: 

303-326.  pis.  17-21.  1890. 


140  MORPHOLOGY  OF  ANGIOSPERMS 

19.  GUIGNARD,  L.     Nouvelles  etudes  sur  la  fecondation.    Ann.  Sci. 

Nat.  Bot.  VII.  14 :  163-296.  pis.  9-18.  1891. 

20.  CHAUVEAUD,  G.  L.    Sur  la  fecondation  dans  les  cas  de  polyembry- 

onie.     Compt.  Rend.  114:  504.  1892. 

21.  GOLINSKI,  ST.  J.    Ein  Beitrag  zur  Entwicklungsgeschichte  des  An- 

droeceums  und  des  Gynaeceums  des  Graser.  Bot.  Centralbl.  55 : 
1-17,  65-72,  129-135.  pis.  1-3.  1893. 

22.  MOTTIER,  D.  M.    Development  of  the  Embryo-sac  in  Acer  rubrum. 

Bot.  Gazette  18:  375-377.  pi.  34.  1893. 

23.  HUMPHREY,  J.  E.    Nucleolen  und  Centrosomen.    Ber.  Deutsch. 

Bot.  Gesell.  12:  108-117.  pi.  6.  1894. 

24.  BELAJEFF,  W.    Zur  Keniitniss  der  Karyokinese  bei  den  Pflanzen. 

Flora.  Erganzungsband,  1894. 

25.  STRASBURGER,  E.    Karyokinetische  Probleme.    Jahrb.  Wiss.  Bot. 

28 :  151-204.  pis.  2-3.  1895. 

26.  MOTTIER,  D.  M.    Beitrage  zur  Kenntniss  der  Kerntheilung  in  den 

Pollenmutterzellen  einiger  Monokotylen  und  Dik'otylen.  Jahrb. 
Wiss.  Bot.  30 :  169-204.  pis.  3-5.  1897. 

27.  CAMPBELL,  D.  H.    The  Structure  and  Development  of  the  Mosses 

and  Ferns.     London  and  New  York.  1895. 

28.  SCHAFFNER,  J.  H.    The  Embryo-sac  of  Alisma  Plantago.    Bot. 

Gazette  21 :  123-132.  pis.  9-10.  1896. 

29.  CAMPBELL,  D.  H.    A  Morphological  Study  of  Naias  and  Zannichel- 

lia.     Proc.  Calif.  Acad.  Sci.  III.  1 :  1-62.  pis.  1-5.  1897. 

30.  CHAMBERLAIN,  C.  J.    Contribution  to  the  Life  History  of  Salix. 

Bot.  Gazette  23 :  147-179.  pis.  12-18.  1897. 

31.  SCHAFFNER,  J.  H.    Contribution  to  the  Life  History  of  Sagittaria 

variabilis.    Bot.  Gazette  23  :  252-273.  pis.  20-26.  1897. 

32.  CHAMBERLAIN,  C.  J.    Contribution  to  the  Life  History  of  Lilium 

Philadelphicum ;  the  Pollen  Grain.  Bot.  Gazette  23:  423-430. 
pis.  35-36.  1897. 

33.  JUEL,  H.  O.    Die  Kerntheilungen  in  den  Pollenmutterzellen  von 

Hemerocallis  fulva  und  die  bei  denselben  auftretenden  Un- 
regelmassigkeiten,  Jahrb.  Wiss.  Bot.  30:  205-226.  pis.  6-8. 
1897. 

34.  SCHAFFNER,  J.  H.    The  Development  of  the  Stamens  and  Carpels 

of  Typha  latifolia.    Bot.  Gazette  24:  93-102.  pis.  4-6.  1897. 

35.  LAWSON,  A.  A.     Some  Observations  on  the  Development  of  the 

Karyokinetic  Spindle  in  the  Pollen  Mother  -  cells  of  Cobaea 
scandens.  Proc.  Calif.  Acad.  Sci.  III.  1 :  169-184.  pis.  33-36. 
1898. 

36.  BELAJEFF,  W.     Die  verwandtschaftlichen  Beziehungen  zwischen 

den  Phanerogamen  und  den  Cryptogamen  in  Lichte  der  neues- 
ten  Forschungen.  Biol.  Centralbl.  18 :  209-218.  1898. 

37.  COULTER,  J.  M.     Contribution  to  the  Life  History  of  Ranunculus. 

Bot.  Gazette  25 :  73-88.  pis.  4-7.  1898. 


THE  MALE  GAMETOPHYTE  141 

38.  CHAMBERLAIN,  C.  J.    Winter  Characters  of  Certain  Sporangia. 

Bot.  Gazette  25:  124-128.  pi  11.  1898. 

39.  SMITH,  E.  W.    A  Contribution  to  the  Life  History  of  the  Ponte- 

deriaceae.     Bot.  Gazette  25 :  324-337.  pis.  19-20.    1898. 

40.  LYON,  FLORENCE   M.     A  Contribution  to  the  Life  History  of 

Euphorbia  corollata.      Bot.   Gazette   25:   418-426.   pis.  22-24. 
1898. 

41.  STEVENS,  W.  C.     The  Behavior  of  the  Kinoplasm  and  Nucleolus 

in  the  Division  of  the  Pollen  Mother-cells  of  Asclepias  Comuti. 
Kansas  Univ.  Quarterly  7:  77-85.  pi.  15.  1898. 

42.  CALDWELL,  O.  W.    On  the  Life  History  of  Lemna  minor.    Bot. 

Gazette  27 :  37-66.  figs.  59.  1899. 

43.  CAMPBELL,  D.  EL    Notes  on  the  Structure  of  the  Embryo-sac  in 

Sparganium  and  Lysichiton.    Bot.  Gazette  27:   153-166.  pi.  1. 
1899. 

44.  FULLMER,  E.  L.    The  Development  of  the  Microsporangia  and  Mi- 

crospores  of  Hemerocallis  fulva.    Bot.  Gazette  28 :  81-88.  pis. 
7-8.  1899. 

45.  WIEGAND,  K.  M.    The  Development  of  the  Microsporangium  and 

Microspores  in  Convallaria  and  Potamogeton.     Bot.  Gazette  28 : 
328-359.  pis.  21r-25.  1899. 

46.  CANNON,  W.  A.    A  Morphological  Study  of  the  Flower  and  Em- 

bryo of  the  Wild  Oat,  Avena  fatua.    Proc.  Calif.  Acad.  Sci.  III. 
1 :  329-364.  pis.  49-53.  1900. 

47.  DUGGAR,  B.  M.    Studies  in  the  Development  of  the  Pollen  Grain  in 

Symplocarpus  foetidus  and  Peltandra  undulata.    Bot.  Gazette 
29 :  81-98.  pis.  1-2.  1900. 

48.  MERRELL,  W.  D.    A  Contribution  to  the  Life  History  of  Silphium. 

Bot.  Gazette  29:  99-133.  pis.  3-10.  1900. 

49.  JOHNSON,  D.  S.    On  the  Endosperm  and  Embryo  of  Peperomia 

pellucida.    Bot.  Gazette  30 :  1-11.  pi.  1.  1900. 

50.  JUEL,  H.  O.    Beitrage  zur  Kenntniss  der  Tetradenbildung.    Jahrb. 

Wiss.  Bot.  35:  626-659.  pis.  15-16.  1900. 

51.  LOTSY,  J.  P.    Rhopalocnemis  phalloides  Jungh.,  a  Morphological- 

systematical  Study.    Ann.  Jard.  Bot.  Buitenzorg  II.  2 :  73-101. 
pis.  3-14.  1900. 

52.  BYXBEE,  EDITH.    The  Development  of  the  Karyokinetic  Spindle 

in  the  Pollen  Mother-cell  of  Lavatera.    Proc.  Calif.  Acad.  Sci. 
III.  2:  63-82.  pis.  10-13.  1900. 

53.  THOMAS,  ETHEL  M.    On  the  Presence  of  Vermiform  Nuclei  in  a 

Dicotyledon.     Annals  of  Botany  14:  318-319.  1900. 

54.  STRASBURGER,   E.     Einige   Bemerkungen  zu  der  Pollenbildung 

bei  Asclepias.     Ber.  Deutsch.  Bot.  Gesell.  19:  450-461.  pi.  2^. 
1901. 

55.  SCHAFFNER,  J.  H.    A  Contribution  to  the  Life  History  and  Cy- 

tology of  Erythronium.    Bot.  Gazette  31 :  369-387.  pis.  4-9.  1901. 


142  MORPHOLOGY  OF  ANGIOSPERMS 

56.  FRYE,  T.  C.    Development  of  the  Pollen  in  some  Asclepiadaceae. 

Bot.  Gazette  32 :  325-331.  pi.  13.  1901. 

57.  ROSENBERG,  O.    Ueber  die  Pollenbildung  von  Zostera.    Meddel. 

Stockholms  Hogsk.  Bot.  Inst.  pp.  21.  1901. 

58.  GAGER,  C.  S.    The  Development  of  the  Pollinium  and  Sperm  Cells 

in  Asclepias  Cornuti.    Annals  of  Botany  16:   123-148.  pi.  7. 
1902. 

59.  GUIGNARD,  L.    La  double  fecondation  chez  les  Solanees.    Jour. 

Botanique  16:  14-5-167.  figs.  45.  1902. 

60.  CHEAUVEAUD,  G.  L.    De  la  reproduction  chez  le  dompte-venin. 

Diss.  Paris.  1902. 


CHAPTER    VII 

FERTILIZATION 

IN  various  ways  the  male  gametophyte  reaches  the  stigma. 
The  literature  dealing  with  pollination  has  become  very  exten- 
sive, and  can  not  even  be  recapitulated  here,  especially  as  it  is 
an  ecological  subject.  The  development  of  tubes  from  pollen- 
grains  lodged  upon  stigmas  has  long  been  known,  but  the  rela- 
tion of  the  tubes  to  fertilization  was  long  misunderstood.  An 
historical  account  of  the  early  views  of  fertilization  among  An- 
giosperms,  together  with  the  citation  of  literature,  was  given 
by  Schacht1  in  1850,  and  by  Hofmeister 2  in  1851..  A  few 
notes  from  Schacht's  account  may  not  be  without  interest,  and 
the  reproduction  of  some  of  his  figures  will  serve  to  show  the 
technique  of  the  time  and  to  illustrate  how  theories  may  in- 
fluence interpretation  (Fig.  65). 

In  1681  !Malpighi  discovered  the  ovule  and  the  embryo- 
sac,  and  also  examined  the  pollen,  but  regarded  it  as  a  useless 
secretion.  Xo  important  advance  was  made  until  1823,  when 
Amici  discovered  the  pollen-tube  on  the  stigma  of  a  Poriulaca 
and  succeeded  in  tracing  the  tube  to  the  ovule.  In  1826  Bron- 
gniart  traced  the  pollen-tube  in  many  plants,  and  in  Pepo 
macrocarpus  saw  hanging  from  the  micropyle  the  end  of  the 
tube  that  had  passed  into  the  embryo-sac ;  "  but,"  says  Schacht, 
"  he  misinterpreted  the  phenomenon,  for  he  regarded  the  pol- 
len-tube as  a  fertilizing  tube  through  which  the  fertilizing  con- 
tents were  brought  to  the  embryo-sac,  there  to  be  taken  up  by 
the  '  embryonal  vesicle/  a  cell  arising  in  the  sac."  In  1826 
Robert  Brown  described  the  development  of  the  integuments, 
and  later  traced  the  pollen-tubes  of  orchids  and  asclepiads  from 
the  stigma  to  the  micropyle.  In  1833  the  knowledge  of  the 
subject  may  be  summarized  as  follows:  there  had  been  observed 

143 


144 


MORPHOLOGY  OF  ANGIOSPERMS 


the  pollen-grain  with  its  pollen-tube  and  some  contents,  as  well 
as  the  ovule  with  its  integuments  and  embryo-sac;  and  the 
pollen-tube  had  been  traced  from  the  stigma  to  the  embryo-sac. 


FIG.  65. — A- C,  Orchis  Morio\  D,  O.  latifolia;  E,  0.  maculata;  F,  Canna  limbata. 
A-B,  young  ovules,  x  150;  (7,  end  of  pollen-tube  enlarging,  x  100;  Z>,  later  stage 
with  two  nuclei  visible  in  embryo,  x  166;  E,  more  advanced  embryo,  x  208;  F, 
considerably  later  stage,  x  125. — After  SCHACHT.! 

In  1835  Schleiden,  the  founder  of  the  cell-theory,  traced 
the  pollen-tube  in  a  large  number  of  widely  separated  families. 
He  claimed  to  have  seen  the  tube  enter  the  micropyle,  press  into 
the  embryo-sac,  and  then  become  itself  the  embryonal  vesicle, 
the  beginning  of  the  embryo.  He  thought  that  the  contents  of 
the  pollen-tube  not  only  give  rise  to  the  embryonal  vesicle,  but 
that  the  end  of  the  tube,  nourished  by  the  embryo-sac,  becomes 
the  future  plant. 


FERTILIZATION 


145 


In  1842  Hartig  described  an  "  egg  "  in  the  embryo-sac,  and 
claimed  that  the  pollen-tube  carries  a  substance  that  fertilizes 
the  egg,  a  view  which  Schleiden  promptly  opposed.  In  the 
same  year  Aniici  reiterated  his  previous  views  and  claimed  for 
Orchis  and  other  plants  the  preexistence  in  the  embryo-sac  of 
a  cell  which,  through  the  influence  of  the  pollen-tube,  becomes 
the  embryo.  Schacht  opposed  this  claim,  and  suggested  that 
such  antiquated  ideas  be  abandoned.  At  the  same  time,  Hugo 
von  Mohl  described  the  egg-apparatus  in  Orchis  Morio,  and 
warmly  supported  Amici's  views. 

In  his  conclusion  Schacht  says :  "  The  tendency  to  error  is 
so  bound  up  in  human  nature  that  the  work  of  one's  mind,  like 
that  of  his  hand,  is  never  perfect,  and  consequently  I  do  not 
consider  my  work  free  from  error  and  misconception,  but  I  have 
tried  to  minimize  these  as  much  as  possible.  In  the  chief 


c 


D 


FIG.  66. — A,  Staphylea ;  tip  of  pollen-tube  showing  division  of  generative  nucleus.  B, 
Orchis  latifolia ;  end  of  pollen-tube  showing  tube  nucleus  (in  advance)  and  the 
two  male  nuclei.  <?,  Monotropa  Bypopitys\  fusion  of  sex  nuclei,  male  nucleus 
more  deeply  shaded.  7>,  the  same  stage  just  after  fertilization,  showing  first  division 
of  endosperm  nucleus,  x  450. — After  SxRASBURGER.8 

matter,  the  origin  of  the  embryo  from  the  pollen-tube,  no  one 
can  convince  me  that  there  has  been  any  error  or  misconcep- 


146  MORPHOLOGY  OP  ANGIOSPERMS 

tion."  Nevertheless,  in  his  text-book,  published  a  few  years 
later,  he  says  that  "  fertilization  "  is  accomplished  in  plants, 
as  in  animals,  by  the  union  of  male  and  female  elements. 

It  is  only  since  1875  that  detailed  information  has  gradu- 
ally accumulated;  and  not  until  1884  (Strasburger  8)  were  the 
cells  concerned  in  fertilization  clearly  pointed  out  (Fig.  66). 

The  tube-cell  of  the  pollen-grain  in  various  ways  pushes 
through  the  exine  a  papillate  protrusion  of  the  intine  that 
develops  into  the  pollen-tube  with  greater  or  less  rapidity. 
Crowding  among  the  loose  papillate  cells  of  the  stigma,  the 
elongating  tubes  enter  the  conducting  tissue  of  the  style.  Ordi- 
narily the  style  is  solid,  and  the  tubes  grow  along  the  conducting 
strand,  which  they  disorganize  more  or  less,  obtaining  from  it 
their  nutritive  supply.  In  case  there  is  a  stylar  canal  the  tubes 
either  pass  down  it,  as  in  Pontederia  (Smith28)  and  Erythro- 
nium  (Schaffner  51),  nourished  by  the  lining  glandular  cells, 
or  they  may  penetrate  the  stylar  tissue  about  the  tube,  as  in 
Campanula  (Barnes9)  and  Juglans  (Nawaschin  20).  In  many 
cases  the  tube  enters  the  ovary  cavity  close  to  the  micropyle; 
in  others  it  must  traverse  more  or  less  of  the  cavity,  being 
"  guided  "  to  the  micropyle  by  various  mechanical  and  nutri- 
tive contrivances. 

Although  ordinarily  pollen-tubes  are  developed  only  in  con- 
tact with  the  stigma,  in  cleistogamous  flowers  tubes  have  been 
observed  issuing  from  pollen-grains  still  in  the  anther,  the  tips 
being  directed  toward  the  stigma.  In  Asclepias  also  multi- 
tudes of  tubes  sometimes  start  from  the  unremoved  pollinia. 

The  time  elapsing  between  pollination  and  fertilization,  as 
inferred  from  the  presence  of  pollen-tubes  in  the  embryo-sac, 
is  extremely  variable,  and  seems  to  hold  no  relation  to  the  dis- 
tance traversed,  as  shown  by  Hofmeister,3  in  comparing  Crocus, 
in  which  a  style  6  to  10  cm.  long  was  traversed  in  one  to  three 
days,  with  Arum,  in  which  a  style  only  2  to  3  mm.  long  was 
traversed  in  five  days.  The  range  in  time  is  probably  repre- 
sented by  the  following  illustrations:  In  Limnocharis  emargi- 
nata  Hall 57  found  a  two-celled  embryo  in  material  killed 
eighteen  hours  after  pollination,  and  thinks  that  in  this  case 
fertilization  probably  occurs  the  first  night  after  pollination. 
Probably  the  most  accurate  estimate  of  the  time  is  that  by 
Mottier  26  for  Lilium,  in  which  the  time  between  artificial  pol- 


FERTILIZATION  147 

lination  and  fertilization  (as  shown  by  fusion)  was  sixty-five  to 
seventy-two  hours.  Guignard  56  has  recorded  an  interval  of  two 
days  between  pollination  and  fertilization  in  Nicotlnana  Taba- 
cum.  Juel  °3  found  by  artificial  pollination  that  fertilization 
occurs  in  Cynomorium  four  days  after  pollination,  sixteen 
days  after  pollination  embryos  of  various  sizes  being  found. 
Hofmeister 2  noted  the  interval  as  one  to  three  days  in 
Crocus,  five  days  in  Arum,  from  ten  days  to  several  months 
among  the  Orchidaceae,  and  in  Colchicum  autumnale  not  less 
than  six  months  (Xovember  to  May).  In  the  last  case,  as  is 
well  known,  pollination  sometimes  occurs  before  there  is  any 
appearance  of  ovules.  Miss  Benson  15  found  three  weeks  elaps- 
ing in  Fagus  sylvatica  between  pollination  and  the  entrance  of 
the  tube  into  the  embryo-sac,  and  the  same  interval  is  reported 
by  D'Hubert 1T  for  certain  Cactaceae.  In  Hamamelis  virgini- 
ana  Shoemaker  62  has  found  that  pollination  occurs  from  Octo- 
ber to  December;  that  the  tubes  develop  at  once  and  grow 
rapidly  until  cold  weather ;  that  during  January  and  February 
the  tube  may  be  found  safely  embedded  in  the  hairy  part  of  the 
carpel ;  and  that  growth  is  resumed  in  the  spring,  fertilization 
occurring  about  the  middle  of  May,  five  to  seven  months  after 
pollination.  The  pollen-grains  of  Hamamelis  show  great  resist- 
ance to  low  temperature,  Shoemaker  citing  cases  in  which  they 
produced  tubes  after  exposure  to  a  week  of  cold,  the  tempera- 
ture sometimes  being  as  low  as  — 15°  C.  Among  the  Amentif- 
erae,  however,  the  interval  becomes  even  more  extended.  Miss 
Benson15  reports  that  it  is  one  month  in  Belula  alba,  two 
months  in  Carpinus  Betulus,  three  months  in  Alnus  glutinosa, 
four  months  in  Corylus  Avellana  and  Quercus  Robur,  and  as 
much  as  eleven  months  in  certain  other  oaks ;  while  in  Q.  velu- 
tina  Conrad  36  found  the  interval  between  pollination  and  fer- 
tilization to  be  thirteen  months.  Baillon  had  long  before  noted 
that  no  indication  of  ovules  is  present  in  Quercus  at  the  time 
of  pollination.  Goebel 10  ha?  associated  these  long  intervals 
with  the  woody  habit,  citing  Ulmus,  Quercus,  Fagus,  Juglans, 
Citrus,  Aesculus,  Acer,  Cornus,  and  Robinia  as  illustrations, 
and  stating  that  the  interval  is  almost  a  year  in  American  oaks 
that  take  two  years  to  ripen  their  seed.  Such  cases  bear  a 
striking  resemblance  in  this  regard  to  many  Gymnosperms. 

A  recent  study  of  Monotropa  uniflora  by  Shibata  65  indi- 


148  MORPHOLOGY   OF  ANGIOSPERMS 

cates  that  the  interval  between  pollination  and  fertilization  in 
any  given  species  may  be  dependent  upon  temperature.  In  the 
case  of  Monotropa,  under  normal  conditions  fertilization  takes 
place  about  five  days  after  pollination ;  but  by  lowering  the  tem- 
perature the  interval  is  lengthened,  and  at  8-10°  C.  fertilization 
is  prevented.  In  Shibata's  experiments  it  was  shown  that 
light,  atmospheric  pressure,  and  mechanical  injury  seem  to 
exert  no  influence  upon  fertilization  and  subsequent  phenomena, 
but  that  the  structures  of  the  embryo-sac  are  very  sensitive  to 
temperature. 

In  a  long  pollen-tube,  or  in  one  that  persists  for  a  long  time, 
it  is  common  to  observe  the  formation  of  successive  cellulose 
plugs  (Prop fen)  that  shut  off  the  growing  tip,  with  its  cells 
and  nuclei,  from  the  cavity  behind,  as  fully  described  by  Stras- 
burger  4  and  Elfving.6  Sometimes  the  plugs  are  so  large  and 
persist  in  such  a  series  that  they  become  conspicuous  objects, 
as  in  Gymnadenia  conopsea  (Marshall-Ward7),  Campanula 
americana  (Barnes9),  Barcodes  sanguinea  (Oliver11),  etc.  In 
such  forms  as  the  Amentiferae  and  others,  in  which  the  tube 
and  its  contents  remain  imbedded  in  the  stylar  tissue  for  a 
period  varying  from  one  month  to  over  a  year,  the  tip  of  the 
tube  is  cut  off  by  a  plug,  its  wall  thickens,  and  it  passes  into 
what  might  fairly  be  called  an  encysted  condition,  as  suggested 
by  Miss  Benson  15  in  connection  with  Carpinus. 

The  branching  of  pollen-tubes,  so  conspicuous  a  phenome- 
non among  Gymnosperms,  is  also  found  among  certain  Angio- 
sperms.  Hofmeister  3  observed  branching  tubes  among  Mono- 
cotyledons in  Potlios  longifolia  and  Hippeastrum  aulicum. 
Among  the  Amentiferae  it  seems  to  be  very  common,  Miss 
Benson15  observing  forking  tubes  in  several  of  the  genera 
(Corylus,  Carpinus,  etc.)  she  studied,  and  in  Quercus  a  cluster 
of  short  branches  at  the  end  of  the  tube ;  while  ^awaschin  20>  3( 
states  that  the  tubes  of  Juglans  and  Ulmus  branch  profusely, 
and  recently  a  similar  branching  has  been  noted  by  Billings  6€ 
in  Gary  a  (Hicoria).  Zinger  31  also  described  the  pollen-tubes 
of  the  Cannabineae  as  ending  in  numerous  swollen  sac-like 
branches.  The  breaking  up  of  the  tip  of  the  tube  into  short 
branches  is  doubtless  a  common  phenomenon,  probably  associ- 
ated with  the  rhizoidal  habit,  but  free  branching  seems  to  be 
characteristic  chiefly  of  chalazogamic  forms. 


FERTILIZATION 


149 


In  1891  Treub  12  announced  the  phenomenon  of  chalazog- 
amy in  Casuarina.  He  found  the  pollen-tube  penetrating  the 
chalazal  region  of  the  ovule,  instead  of  entering  through  the 
micropyle.  In  this  case  the  pollen-tube  becomes  associated  with 
the  numerous  elongated  sterile  megaspores,  and  doubtless  they 
are  of  service  in  rendering  the  passage  easy;  and  later  it  enters 
the  antipodal  region  of  the  embryo-sac  and  approaches  the  egg- 
apparatus  from  that  direction  (Figs.  67,  24(7).  In  1893 
Xawaschin14  reported  chalazogamy  in  Betula]  and  in  1894 
Miss  Benson  15  not  only  observed  the  phenomenon  in  Betula, 
but  also  added  Ahius,  Corylus,  and  Car pinus  to  the  list  of 
chalazogamic  plants.  In  all  of  these  cases  Miss  Benson  ob- 
served the  tubes  following  a  course 
parallel  with  the  vascular  strands 
of  the  raphe,  thus  reaching  and 
penetrating  the  chalaza.  In  Cory- 
lus and  Carpinus  the  tube  enters 
a  more  or  less  conspicuous  caecum 
developed  in  the  antipodal  region 
of  the  sac,  traverses  it,  and  comes 
in  contact  with  the  egg;  but  in 
.1  hi  us  the  tube  traverses  the  nucel- 
lus  to  the  micropylar  region  above 
the  embryo-sac,  and  then  turns 
and  enters  it  as  though  it  had  come 
by  way  of  the  micropyle.  In  1895 
Xawaschin  20  added  Juglans  cine- 
rea  and  /.  regia  to  the  list.  In  the 
latter  species  the  tube  does  not  pass  down  the  stylar  canal  or 
traverse  the  cavity  of  the  ovary,  but  advances  through  the  tissue 
•  of  the  style  and  of  the  ovary  wall  until  opposite  the  insertion  of 
the  single  ovule  that  fills  the  ovary  cavity.  It  then  leaves  the 
ovary  wall  and  pierces  the  chalaza,  branching  freely  in  the  nu- 
cellus,  which  is  described  as  "  veined  "  by  tubes  surrounding  the 
sac  on  all  sides.  The  male  nuclei  discharged  into  the  sac  were 
seen  "  wandering  "  in  its  cytoplasm  and  fusing  with  one  of  sev- 
eral free  cells  that  function  as  eggs  but  have  not  organized  an  egg- 
apparatus.  Recently  Billings  66  has  discovered  chalazogamy  in 
Gary  a  olivaeformis,  the  common  pecan,  the  details  conforming 
almost  exactly  to  those  given  by  Xawaschin  for  Juglans  regia. 


FIG.  67.  —  Casuarina  suberosa.  A1 
pollen-tube  entering  chalazal  end 
of  embryo-sac,  x  270;  £,  stage 
showing  (TreuVs  interpretation) 
formation  of  endosperm  before  fer- 
tilization, x  180.  After  TBEUB." 


150  MORPHOLOGY  OF  ANGIOSPERMS 

In  1898  Nawaschin  30  described  some  remarkable  variations 
in  the  course  of  the  pollen-tube  in  Ulmus  pedunculata  and  U. 
montana.  In  addition  to  tubes  following  the  ordinary  chala- 
zogamic  route,  some  instead  of  penetrating  the  chalaza  pass 
from  the  funiculus  across  the  short  outer  integument,  and 
thence  into  and  upward  through  the  inner  integument  to  the 
top  of  the  nucellus,  when  they  turn  across  to  the  bottom  of  the 
micropyle  and  so  enter  the  nucellus  from  the  usual  direction ; 
others  follow  the  same  route  except  that  they  pass  directly  from 
the  funiculus  into  the  inner  integument ;  while  still  other  tubes 
branch  profusely  and  apparently  with  no  definiteness  within 
both  the  funiculus  and  integument.  In  the  same  species,  there- 
fore, pollen-tubes  may  enter  the  sac  either  at  the  antipodal  or 
micropylar  ends,  and  may  either  pass  with  great  directness  or 
branch  profusely. 

The  behavior  of  the  pollen-tubes  in  Ulmus  suggested  that 
there  might  be  other  routes  than  through  the  micropyle  or 
through  the  chalaza,  and  this  has  been  observed  in  other  forms. 
In  his  study  of  the  Cannabineae  in  1898,  Zinger  31  discovered 
that  the  two  thick  integuments  completely  coalesce  over  the 
apex  of  the  nucellus,  and  the  micropyle  is  entirely  closed  by 
tissue.  The  pollen-tube  either  bores  its  way  through  the  tissue 
filling  the  micropyle  or  pierces  the  two  integuments,  reaching 
the  nucellus  and  branching  about  its  apex,  and  finally  sending 
one  very  slender  branch  into  the  embryo-sac. 

With  these  facts  before  them,  Pirotta  and  Longo 41  pro- 
posed the  term  "  acrogamy  "  for  the  entrance  of  the  pollen-tube 
directly  through  the  micropyle ;  "  basigamy  "  for  its  entrance 
through  the  chalaza  (Casuarina,  Betula,  Alnus,  Corylus,  Carpi- 
nus,  Juglans,  and  sometimes  Ulmus)  ;  and  "  mesogamy  "  for 
its  entrance  by  intermediate  routes  (sometimes  Ulmus,  and 
Cannabineae).  In  the  following  year  Longo  49  described  a  case 
of  mesogamy  in  Cucurbita,  in  which  the  pollen-tube  traverses 
the  tissues  of  the  funiculus  and  outer  integument  before  enter- 
ing the  micropyle.  Practically  the  same  phenomenon  has  been 
observed  by  Murbeck  50  in  Alchemilla  arvensis,  in  which  the 
micropyle  is  entirely  closed  by  the  growth  of  the  integument, 
and  the  pollen-tube  enters  the  ovule  at  the  chalazal  end,  trav- 
erses the  entire  length  of  the  integument  within  its  tissues,  and 
thus  enters  the  micropylar  extremity  of  the  embryo-sac. 


FERTILIZATION  151 


True  chalazogamy,  therefore,  has  as  yet  been  found  only 
among  the  Amentiferae,  but  such  an  intermediate  condition 
as  shown  by  Ulmus,  Cucurbita,  and  Alchemilla,  in  which  the 
pollen-tube  enters  the  ovule  at  the  chalazal  end,  but  traverses 
the  integument  instead  of  the  nucellus,  suggests  that  chala- 
zogamy is  an  exceptional  condition  derived  from  the  ordinary 
route  of  the  pollen-tube  through  the  micropyle.  In  certain 
cases  the  tube  reaches  the  micropyle  by  passing  along  more  or 
less  of  the  surface  of  the  integument;  in  other  cases  it  enters 
the  tissues  of  the  integument,  and  finally  it  penetrates  deeper, 
entering  the  chalazal  tissue.  This  seems  to  be  a  natural 
sequence  of  events  that  resulted  in  chalazogamy,  which  there- 
fore \vould  hold  no  relation  to  a  primitive  condition  of  Angio- 
sperms  or  to  their  classification. 

In  passing  through  the  micropyle  the  pollen-tube  is  more 
or  less  compressed,  and  upon  reaching  the  wall  of  the  embryo- 
sac  may  broaden  out  upon  it.  In  some  cases  (p.  94)  the 
synergids  have  already  pierced  the  wall  of  the  embryo-sac,  but 
in  most  cases  it  must  be  pierced  by  the  tube.  Upon  entering  the 
sac  the  tube  either  passes  between  the  synergids,  as  in  Ponte- 
deria  (Smith28),  Euphorbia  (Lyon29),  sometimes  Salix 
(Chamberlain23),  etc.  (Fig.  44)  ;  or  between  the  sac-wall  and 
one  synergid,  as  in  Alisma  (Schaffner  22),  Lilium  (Coulter25), 
Ranunculus  (Coulter27),  Fagus  (Benson15),  Silphium  (Mer- 
rell35),  etc.  Recently,  however,  Guignard  56  has  reported  that 
in  Nicotiana  Tabacum  and  Datura  laevis  the  tube  passes  into 
a  synergic!  and  discharges  its  contents  into  the  broken-up  body. 
So  far  as  our  own  observation  goes,  the  usual  route  of  the  tube 
is  between  the  sac-wall  and  one  of  the  synergids,  but  this  may 
well  vary  even  in  the  same  species.  Within  the  sac  the  tip 
of  the  tube  usually  becomes  much  swollen,  often  appearing 
pouch-like,  as  in  Alisma,  Erythronium,  Ranunculus,  Silphium, 
etc.,  due  probably  to  the  rapid  absorption  of  material  from  the 
synergid.  As  a  rule,  one  synergid  is  disorganized  by  its  contact 
with  the  tube;  but  in  Salix  (Chamberlain23)  (Fig.  44),  Sil- 
pliium  (Merrell85),  Nigella  (Guignard53),  etc.,  cases  of  fer- 
tilization have  been  observed  in  which  both  synergids  remained 
intact;  while  in  Erigeron  (Land38)  both  synergids  are  fre- 
quently disorganized.  D'Hubert 17  has  made  the  interesting 
observation  in  connection  with  his  study  of  the  Cactaceae  that 
11 


152 


MORPHOLOGY  OF  ANGIOSPERMS 


the  nucleus  of  one  synergid  moves  toward  the  tube  upon  its 
entrance  into  the  sac,  and  that  the  nucleus  of  the  other  synergid 
moves  toward  the  nucleus  of  the  egg. 

In  case  the  tube  passes  between  the  synergids  it  advances 
directly  toward  the  egg-nucleus ;  but  in  case  it  passes  along  the 
wall  of  the  sac  the  tip  of  the  tube  curves  toward  the  egg-nucleus. 
In  any  event,  the  tip  of  the  tube,  in  which  a  thin  area  (pit) 

is  developed,  is  directed  toward 
the  egg-nucleus  when  the  dis- 
charge takes  place.  Under  the 
pressure  developed  by  the  turgor 
of  the  end  of  the  tube,  and  re- 
sisted by  the  small  caliber  of  the 
tube  in  its  passage  through  the 
micropyle  and  sac-wall,  the 
membrane  of  the  pit  is  ruptured, 
and  a  discharge  of  the  contents 
results.  The  perforated  tip  of  the 
pollen-tube,  after  the  discharge, 
has  been  demonstrated  fre- 
quently, as  seen  by  Schaffner  4^ 
in  Sagittaria  (Fig.  68).  The 
discharge  seems  to  be  forcible 
enough  to  empty  the  end  of  the 
tube  of  most  of  its  contents,  the 
most  important  ones  being  the  two  male  nuclei.  Cases  have  been 
reported  in  which  only  one  male  nucleus  is  said  to  be  discharged, 
as  in  Alisma  (Schaffner  22)  and  Sagittaria  (Schaffner  24),  the 
other  being  recognized  as  degenerating  in  the  tube.  However, 
the  frequent  presence  of  disorganizing  bodies  within  the  tube 
after  fertilization  (Fig.  71),  and  numerous  observations  of  the 
discharge  of  both  male  nuclei,  and  especially  the  rapidly  multi- 
plying illustrations  of  "  double  fertilization,"  incline  to  the  be- 
lief that  the  discharge  of  both  male  nuclei  into  the  sac  is  usual. 
The  passage  of  the  male  nucleus  through  the  cytoplasm  of 
the  egg  toward  the  female  nucleus  may  be  attended  by  an 
increase  in  size  and  change  in  form,  but  the  changes  are  not  so 
conspicuous  as  those  that  occur  in  the  male  nucleus  that  passes 
deeper  into  the  sac  to  fuse  with  the  polar  nuclei.  For  example, 
in  Caltha  palustris  Miss  Thomas  44  found  the  male  nuclei  very 


FIG.  68. — Sagittaria  variabilis.  Pollen- 
tube  in  the  act  of  discharging;  four 
centrosomes  represented;  x  900. — 

After   SCHAFFNER.2* 


FERTILIZATION 


small  and  oblong  or  lenticular  on  extrusion,  the  one  passing  to 
the  polar  nuclei  increasing  very  much  in  size,  the  other  very 
little.  In  Tricyrtis  hirta  Ikeda  58  found  the  male  nucleus  that 
passes  to  the  polar  nuclei  showing  "  enormous  change  in  size 
and  shape  "  as  it  passes  through  the  sac.  There  is  usually  more 
or  less  elongation  of  male  nuclei  at  the  time  of  discharge  or 
afterward,  but  in  Monotropa  uniflora  Shibata  54  has  seen  them 
elongated  when  entering  the  sac,  but  becoming  more  nearly 
spherical  as  fusion  progresses.  In  the  pollen-grain  at  the  time 
of  shedding  the  generative  nucleus  stains  blue  and  the  tube 
nucleus  red  with  a  combination  like  cyanin  and  erythrosin. 
This  reaction  is  maintained,  the  male  nucleus  staining  blue 
even  after  coming  into  contact  with  the  nucleus  of  the  egg 
which  stains  red ;  but  as  fusion  proceeds  the  male  nucleus  takes 
less  and  less  of  the  cyanin  and  finally  stains  with  erythrosin 
like  the  nucleus  of  the  egg. 

The  fusion  of  the  male  and  female  nuclei  may  be  very 
rapid,  as  observed  by  Guignard  48j  53  in  Zea  and  Ranuncula- 
ceae ;  or  the  two  may  be  long  in  contact  without  fusion,  as  noted 
by  Johnson37  in  Peperomia.  The  behavior  of  the  chromatin 
during  fusion  has  received  but  little  attention.  Mottier  26  fig- 
ures the  chromatin  when  the  nuclei  are  partly  fused,  and  the 
statement  is  generally  current  that  the  nuclei  fuse  in  the  resting 
condition  (Fig.  69).  In  view  of 
the  independence  of  the  pater- 
nal and  maternal  chromatin  dur- 
ing fertilization  in  Gymno- 
sperms,  as  recently  noted  by 
several  investigators,  it  would  be 
well  to  reexamine  the  subject  in 
Angiosperms,  especially  since 
most  observers  have  paid  little 
or  no  attention  to  this  phase  of 
the  problem. 

Since  it  has  been  in  connec- 
tion with  fertilization  and  at- 
tendant phenomena  that  the  cen- 
trosome  problem  has  come  into 
greatest  prominence,  it  may  not  be  inappropriate  to  refer  to  the 
subject  at  this  point.  Guignard,  Schaffner,  and  others  have 


FIG.  69. — Lilium  candidum.  Fusion  of 
sex  nuclei ;  the  synergids  appear  as 
dense  homogeneous  masses. — After 
MOTTIER." 


154 


MORPHOLOGY  OF  ANGIOSPERMS 


regarded  the  centrosome  as  a  permanent  organ  performing  an 
important  function  in  mitosis  and  in  fertilization.  Even  the 
"  quadrille  of  the  centers/'  described  by  the  zoologist  Fol,  was 
identified  by  these  observers.  Centrosomes  in  the  vascular 
plants  have  been  figured  by  many  other  prominent  botanists, 
including  Humphrey,16  Strasburger,18  Campbell,19  and  Mot- 


D 


FIG.  70. — Figures  of  centrosomes  in  vascular  plants.  A,  Lilium  Martagon,  the  reduction 
division  at  germination  of  megaspore  ;  12  chromosomes  may  be  counted;  x  600; 
after  GUIGNARD.IS  B,  Larix  europaea,  first  division  of  pollen  mother-cell ;  x  600 ; 
after  STRASBURGER. 18  6Y,  Delphinium  tricorne,  first  division  of  megaspore  mother- 
cell;  "at  upper  pole  are  centrospheres " ;  x  588;  after  MorriER.21  /),  Sagittaria 
variabilis,  first  division  of  pollen  mother-cell;  x  640;  after  ScHAFFNER.24  E,  Lilium 
candidum,  reduction  division  at  germination  of  megaspore ;  after  BERNARD.**  F, 
Psilotum  triquetrum,  first  division  of  spore  mother-cell;  x  800;  after  HUMPHREY.1* 
G,  Equisetum  telemateia,  tetrad  of  four  spores ;  x  960 ;  after  CAMPBELL.19 

tier26  (Fig.  70).     Most  botanists,  following  Strasburger,  have 
publicly  renounced  any  belief  in  the  centrosome  as  an  organ  of 


UTILIZATION 


155 


vascular  plants,  and  many  others  have  made  a  tacit  renuncia- 
tion.    To  say  that  all  the  figures  that  have  been  drawn  have 


•Pt 


FIG.  71. — Double  fertilization.  A,  Helianthus  annuus,  showing  the  two  coiled  male 
nuclei,  one  fusing  with  the  egg-nucleus  and  the  other  with  the  endosperm  nucleus ; 
after  NAWAscniN.40  B,  Iris,  the  two  polar  nuclei  not  yet  fused;  after  GuioxARD.32 
(7,  Silphium  laciniatum :  sp^  sp%,  male  nuclei :  0,  oosphere ;  0,  endosperm  nucleus ; 
sy,  synergid ;  pt,  pollen- tube ;  x,  two  conjectural  bodies  often  seen  in  the  pollen- 
tube  after  the  male  nuclei  have  been  discharged ;  x  525  ;  after  LAND.38 

been  mere  products  of  the  imagination  would  be  a  radical  state- 
ment, and  one  doubtless  very  far  from  the  truth.  In  our 
opinion  the  observations,  figures,  and  descriptions,  like  the 
pollen-tube  embryos  of  Schleiden  and  Schacht,  furnish  an  exam- 
ple of  the  extent  to  which  even  a  careful  and  conscientious 
scientist  may  be  influenced  by  preconceived  opinion. 

Our  knowledge  of  the  phenomenon  called  "  double  fertili- 
zation "  (Fig.  71)  dates  from  1898,  when  Nawaschin  S3j  34  an- 


156 


MORPHOLOGY  OF  ANGIOSPERMS 


nounced  at  a  meeting  of  the  Russian  Society  of  Naturalists  in 
August  that  it  occurs  in  Lilium  Martagon  and  Fritillaria  ten- 
ella.  In  1899  Guignard  32  observed  the  same  phenomenon  in 
Lilium  pyrenaicum,  Fritillaria  meleagris,  and  Endymion 
nutans.  During  1900  the  literature  of  the  subject  increased 
rapidly.  Nawaschin 40  added  Juglans,  Delphinium  elatum, 
Rudbeckia  speciosa,  and  Helianthus  annuus  to  the  list,  and  in 
certain  orchids  (Arundina  and  Phajus)  he  found  the  second 
male  nucleus  consorting  with  the  polar  nuclei,  but  there  was  no 
fusion.  Guignard 39  described  the  phenomenon  in  species  of 
Tulipa  (Fig.  72),  also42  in  Scilla,  Narcissus,  Reseda,  and 
Hibiscus ;  and  Strasburger  43  not  only  added  Himantoglossum, 


A 


B 


FIG.  72. — A,  embryo-sac  of  Tulipa  sylvestris,  showing  nuclei  scattered  irregularly,  each 
nucleus  surrounded  by  a  rather  definitely  limited  portion  of  the  cytoplasm ;  x  300. 
J?,  T.  Celsiana,  showing  double  fertilization  in  sac  like  that  shown  in  A ;  the  male 
nuclei  recognized  by  vermiform  appearance ;  x  333. — After  GUIGNAKD." 

certain  species  of  Orchis,  and  Monolropa  Ilypopitys,  but  dis- 
cussed the  whole  subject.  Miss  Thomas  44>  45  reported  double 
fertilization  in  Caltha  palustris ;  Guignard  42  announced  it  in 
Ranunculus  Flammula,  Helleborus  foetidus,  Anem.one  nemo- 
rosa,  Clematis,  Viticella,  and  Nigella  sativa,  and  independently 
confirmed  its  occurrence  in  Caltha  palustris.  Land  38  found  it 
in  species  of  Erigeron  and  Silphium ;  it  was  observed  repeatedly 


FERTILIZATION 

in  this  laboratory  in  Lilium  philadelphicum  (Fig.  36,  H),  L. 
trigrinum,  and  Anemone  patens  Nuttalliana ;  and  at  the  close 
of  1900  Miss  Sargant  46  published  a  resume  and  general  discus- 
sion of  the  subject.  More  recently,  Guignard  48  has  described 
double  fertilization  in  Zea  and  Naias  major',  Land  has  discov- 
ered it  in  Cnicus  and  possibly  in  Taraxacum ;  while  Guignard  53 
has  added  Nigella  damascena  and  Ranunculus  Cymbalaria; 
and  Frye  60  has  described  its  occurrence  in  Asdepias  Cornuti. 
Karsten  55  has  also  confirmed  the  occurrence  of  double  fertili- 
sation in  Juglans,  investigating  several  species ;  Shibata  54  has 
added  Monotropa  uniflora,  Ikeda  58  Tricyrtis  liirta,  Strasbur- 
ger  59  Ceratopliyllum  demersum,  Guignard  56  species  of  Nico- 
tiana  and  Datura,  as  well  as  of  Capsella  and  Lepidiitmf* 
Wylie  67  Elodea,  and  Frye  68  Casuarina. 

It  will  be  seen  that  the  phenomenon  is  not  restricted  to  a 
few  groups,  but  is  widely  displayed  among  both  Monocotyledons 
and  Dicotyledons ;  among  the  former  having  been  observed  in 
Xaiadaceae,  Hydrocharitaceae,  Gramineae,  Liliaceae,  Amaryl- 
lidaceae,  and  Orchidaceae ;  and  among  the  latter  in  Juglanda- 
<?eae,  Ceratophyllaceae,  Ranunculaceae,  Cruciferae,  Resedaceae, 
Malvaceae,  Ericaceae,  Asclepiadaceae,  Solanaceae,  and  Com- 
positae.  Probably  it  is  not  safe  to  infer  the  general  occurrence 
of  double  fertilization,  although  the  observations  already  include 
sixteen  families,  about  forty  genera,  and  over  sixty  species, 
besides  inferential  testimony  in  other  species  from  the  form  and 
activity  of  both  male  nuclei  and  from  the  phenomenon  of  xenia. 
In  any  event,  it  is  common  enough  to  demand  a  general  explana- 
tion of  its  significance,  its  place  in  the  history  of  Angiosperms, 
and  especially  whether  it  is  really  fertilization  or  merely  triple 
fusion.  It  has  certainly  introduced  among  structures  already 
difficult  of  interpretation  a  phenomenon  that  immensely  in- 
creases the  difficulty.  The  subject  will  be  discussed  briefly 
under  endosperm  (Chapter  VIII),  and  only  such  general 
details  presented  here  as  have  been  observed  in  connection  with 
the  process. 

It  is  claimed  by  Guignard  for  Lilium,  and  confirmed  by 
Miss  Thomas  in  Calfha,  that  the  first  male  nucleus  extruded 
from  the  tube  passes  to  the  polar  nuclei.  The  frequently  vermi- 
form and  spiral  character  of  this  nucleus  has  suggested  the  possi- 
bility of  independent  motion ;  but  this  form  is  by  no  means  con- 


158  MORPHOLOGY  OF  ANGIOSPERMS 

stant,  and  Strasburger,43  in  examining  the  process  in  living- 
material  of  Monotropa,  demonstrated  the  passage  of  the  male 
nucleus  in  the  streaming  protoplasm  of  one  of  the  cytoplasmic 
strands  connecting  the  primary  endosperm  nucleus  or  the  polar 
nuclei  with  the  egg-apparatus.  This  is  confirmed  by  Guig- 
nard,53 who  has  described  and  figured  the  very  small  male 
nucleus  passing  down  the  broad  cytoplasmic  strand  that  con- 
nects the  egg-apparatus  with  the  antipodals  and  envelops  the 
primary  endosperm  nucleus  in  Nigella,  Damascena,  Ranunculus- 
Cymbalaria,  and  Anemone  nemorosa,  and  which  is  doubtless 
true  of  the  other  Ranunculaceae.  It  seems  probable  that  the 
male  nucleus  is  generally  carried  along  one  of  these  strands ;  but 
it  is  not  improbable  that  the  vermiform  nuclei  occasionally 
acquire  some  power  of  independent  motion.  It  is  during  this 
passage  that  the  male  nucleus  may  increase  much  in  size 
(Thomas,44  Ikeda58)  and  may  even  assume  the  vermiform 
character;  although  all  such  changes  may  have  occurred  before 
discharge  from  the  pollen-tube,  even  in  the  pollen-grain,  as 
observed  by  Merrell  35  in  Silphium.  The  male  nucleus,  how- 
ever, may  retain  its  small  size  and  oval  form  even  in  contact 
with  the  polar  nuclei,  as  observed  by  Guignard  32  in  Endymion, 
and  by  other  observers  since.  In  Juglans  Karsten  55  believes 
that  in  all  cases  the  polars  are  fertilized  before  the  egg ;  but  in 
Nicotiana  Tabacum  Guignard  56  reports  that  sometimes  the  egg 
is  fertilized  first  and  sometimes  the  polars,  so  that  probably 
there  is  no  definite  order  in  the  two  fusions. 

Every  possible  order  in  the  fusion  of  the  three  nuclei  has 
been  observed,  so  that  the  triple  fusion  is  brought  about  in  a 
variety  of  ways.  As  might  be  expected,  it  is  often  the  case  that 
the  polar  nuclei  have  already  fused  when  the  pollen-tube  enters 
the  embryo-sac,  and  the  male  nucleus  unites  with  the  fusion 
nucleus,  as  in  Tricyrtis,  Ranunculaceae,  Datura,  Erigeron,  Sil- 
phium, etc. ;  although  even  in  this  case  the  polar  nuclei  may  not 
always  lose  their  individuality.  The  two  polar  nuclei  and  the 
male  nucleus  have  also  been  observed  to  fuse  all  together,  as  in 
Zea  (Guignard  48)  and  other  plants,  in  which  the  vermiform 
male  nucleus  seems  to  bind  the  polar  nuclei  together.  In  Nicoti- 
ana (Guignard  56)  the  male  nucleus  comes  in  contact  with  either 
•polar  nucleus  or  both.  In  Lilium  Martagon  the  male  nucleus 
usually  fuses  first  with  the  upper  polar  nucleus,  and  later  the 


FERTILIZATION  159 

lower  polar  nucleus  enters  the  combination,  as  was  also  observed 
by  Shibata  54  in  Monotropa  uniflora]  but  in  Lilium  it  has  been 
observed  that  if  the  lower  polar  nucleus  happens  to  be  the  more 
favorably  placed  the  male  nucleus  fuses  with  it  first.  In  Ascle- 
pias  Cornuti  (Erye60)  both  male  nuclei  are  vermiform  and 
more  or  less  curved,  and  one  of  them  was  observed  in  contact 
with  a  polar  nucleus  near  the  antipodal  cells,  the  micropylar 
polar  nucleus  being  some  distance  away  and  nearer  the  egg- 
apparatus.  That  the  male  nucleus  may  thus  traverse  much  of 
the  embryo-sac  is  also  shown  in  Nigella  damascena  and  Anem- 
one nemorosa,  in  both  of  which  Guignard  53  observed  the  male 
nucleus  uniting  with  the  fusion  nucleus  near  the  prominent 
antipodal  cells. 

At  present  there  is  a  decided  tendency  among  botanists  and 
zoologists  to  distinguish  two  distinct  phenomena  in  fertiliza- 
tion— namely,  the  stimulus  to  growth  and  the  mingling  of  ances- 
tral qualities.  Strasburger  43  regards  the  latter  process  as  the 
essential  one,  and  the  stimulus  to  growth  as  only  providing  the 
conditions  which  make  it  possible  to  obtain  the  advantages 
resulting  from  a  mingling  of  ancestral  plasma  masses.  In  a 
later  paper  59  he  makes  the  statement  that  fluctuating  variations 
do  not  furnish  a  starting-point  for  the  formation  of  new  species, 
but  that  it  is  the  principal  function  of  fertilization,  through 
the  mingling  of  ancestral  plasma  masses,  to  keep  the  species 
characters  constant.  The  essence  of  fertilization  lies  in  the 
union  of  organized  elements.  It  was  to  insure  this  essentially 
generative  fertilization  that,  in  the  course  of  phylogenetic  devel- 
opment, the  inability  of  the  sexual  cells  to  develop  independ- 
ently became  more  and  more  marked.  The  term  generative 
fertilization  is  used  in  contrast  wTith  vegetative  fertilization, 
which  is  merely  a  stimulus  to  growth.  Hence  Strasburger  re- 
gards the  fusion  of  the  male  nucleus  with  the  polar  nuclei  as 
merely  vegetative  fertilization,  and  lacking  the  essential  feature 
of  a  sexual  fusion.  It  is  worthy  of  note  that  Ernst  61  finds  in 
Paris  quadrifolia  and  Trillium  grandiflorum  a  striking  differ- 
ence between  generative  and  vegetative  fertilization,  the  fusion 
of  the  male  nucleus  with  the  egg-nucleus  being  complete,  so 
that  a  typical  resting  nucleus  is  formed ;  while  the  polar  nuclei 
begin  to  form  spirems  even  before  the  male  nucleus  arrives,  and 
in  the  group  of  three  nuclei — the  two  polar  nuclei  and  the  male 


160 


MORPHOLOGY  OF   ANGIOSPERMS 


nucleus — three  spirems  are  distinguishable,  a  case  observed  also 
in  this  laboratory  by  Miss  Laetitia  Snow  in  Lilium  philadel- 
phicum.  In  such  cases  it  is  very  probable  that  there  is  no  union 
of  the  chromatin  (Fig.  73),  and  it  is  known  that  in  Pinus  there 
is  no  fusion  of  the  chromatin  of  the  two  sex  nuclei  before  the 


ffigip^ 
/**&( 


FIG.  73. — Paris  quadrifolia.  A,  two  polar  nuclei  in  spirem  stage ;  male  .nucleus  (ra) 
shown  just  above ;  B,  the  two  nuclei  and  male  nucleus  in  spirem  stage ;  x  1250.— 
After  ERNST." 

binucleate  stage  of  the  proembryo  is  reached,  and  the  majority 
of  published  figures  show  this  condition.  However,  Land 3* 
describes  a  complete  fusion  of  the  polar  nuclei  of  Silphium 
before  the  union  with  the  second  male  nucleus. 

On  the  whole,  it  is  to  be  regretted  that  the  phrase  "  double 
fertilization  "  has  been  applied  to  this  phenomenon,  since  it  is 
far  from  established  that  it  is  to  be  regarded  as  real  fertiliza- 
tion. During  this  uncertainty  it  would  seem  convenient  and 
sufficient  to  speak  of  it  as  "  triple  fusion."  It  is  also  mislead- 
ing to  speak  of  the  vermiform  male  nuclei  as  "  antherozoids  " 
or  "  spermatozoids  "  in  the  sense  that  they  are  something  mor- 
phologically distinct  from  the  other  male  nuclei  of  Angiosperms. 
Whatever  the  ordinary  male  nuclei  of  Angiosperms  may  be  these 
vermiform  nuclei  are.  Probably  male  cells  are  always  organ- 
ized, and  we  consider  them  as  morphologically  sperm  mother- 
cells;  but  it  is  also  probable  that  only  the  male  nuclei  become 


FERTILIZATION 

vermiform  and  take  part  in  fusion.  In  preparations  of  Lilium 
we  have  seen  a  vermiform  nucleus  still  enclosed  by  the  cyto- 
plasm of  the  male  cell.  It  would  be  strange  morphology  to  base 
the  definition  of  a  sperm-cell  upon  its  form  or  power  of  inde- 
pendent motion. 

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lished in  Bot.  Gazette  35:  1903. 


CHAPTER    VIII 


THE    ENDOSPERM 

THE  endosperm  of  Gymnosperms  seems  to  be  clearly  the 
vegetative  tissue  of  the  female  gametophyte,  but  the  morpho- 
logical nature  of  the  endosperm  of  Angiosperms  (Fig.  74)  is  not 
so  clear.  The  ger- 
mination of  the 
megaspore  begins, 
as  in  Gymnosperms, 
with  free  and  simul- 
taneous nuclear  di- 
vision. In  Gymno- 
this 


sperms 
tinues 
time     and 
placed    by 


for 


con- 
some 
is     re- 
cell-for- 


mation, giving  rise 
to  an  extensive  tis- 
sue bearing  arche- 
gonia,  while  in  ^i- 
giosperms  usually 
only  eight  free  nu- 
clei are  formed  be- 
fore an  egg  is  organ- 
ized and  fertiliza- 
tion takes  place.  In 
both  cases  endo- 
sperm is  formed 
after  fertilization;  but  in  Gymnosperms  it  is  a  continuation 
of  cell  division,  while  in  Angiosperms  it  usually  begins  with 
nuclear  fusion  followed  by  simultaneous  and  often  free  nuclear 

165 


A 


FIG.  74. — Two  modes  of  initiating  the  formation  of  endo- 
sperm. A,  Ifaias  major,  illustrating  free  nuclear  divi- 
sion ;  there  are  four  free  nuclei  belonging  to  the  endo- 
'  sperm,  the  lower  free  nucleus  being  that  of  the  upper 
antipodal ;  x  175.  B,  Datura,  laevis,  nuclear  division 
followed  immediately  by  formation  of  wall ;  x  225. — 


166  MORPHOLOGY  OF  ANGIOSPERMS 

division.  This  nuclear  fusion  is  one  of  the  most  striking  fea- 
tures of  the  Angiosperms  as  contrasted  with  Gymnosperms,  and 
especially  since  the  discovery  of  so-called  "  double-fertilization  " 
the  morphological  character  of  the  endosperm  of  Angiosperms 
is  in  question.  For  this  reason,  we  have  preferred  to  discuss 
it  apart  from  the  gametophytic  structures  concerning  which 
there  is  no  question. 

As  has  been  said,  the  endosperm  of  Angiosperms  is  usually 
derived  from  a  fusion  nucleus,  the  constituent  members  being 
the  micropylar  polar  nucleus,  sister  to  the  egg,  and  the  antipo- 
dal polar  nucleus.  If  the  current  homologies  are  true,  this 
fusion  is  that  of  a  female  and  a  vegetative  nucleus.  In  many 
cases  a  male  nucleus  also  joins  in  the  structure  of  the  primary 
endosperm  nucleus,  which  is  then  the  result  of  a  triple  fusion 
(Figs.  36,  H,  and  71-73).  How  far  this  male  nucleus  is  an  es- 
sential factor  in  the  formation  of  the  endosperm  of  Angiosperms 
is  at  present  unknown,  but  the  rapidly  increasing  number  of 
plants  in  which  triple  fusion  has  been  observed  leads  to  the 
belief  that  it  may  be  of  general  occurrence.  It  should  also  be 
remembered  that  in  Peperomia  pellucida  (Johnson31)  (Fig. 
38)  the  primary  endosperm  nucleus  is  the  result  of  the  fusion 
of  no  less  than  eight  of  the  sixteen  free  nuclei  of  the  embryo- 
sac;  and  that  in  Gunnera  (Schnegg47)  (Fig.  39)  the  same  sort 
of  multiple  fusion  occurs.  The  fusion-nucleus,  therefore,  may 
be  made  up  of  a  variable  number  of  constituents  of  various 
morphological  character,  and  hence  the  significance  of  the 
fusion  and  the  nature  of  the  resulting  tissue  are  peculiarly  dim- 
cult  to  interpret. 

While  the  fusion  of  these  nuclei  seems  to  result  in  what  has 
been  called  a  growth-stimulus,  endosperm  is  sometimes  formed 
without  any  antecedent  fusion.  For  example,  in  Balanophora 
(Treub,16  Lotsy26)  the  polar  nuclei  do  not  fuse,  but  divide 
independently,  the  embryo-sac  becoming  filled  with  endosperm 
tissue;  and  in  Helosis  (Chodat  and  Bernard33)  after  the  first 
division. of  the  nucleus  of  the  megaspore  the  chalazal  nucleus 
disintegrates  so  that  antipodal  cells,  and  hence  an  antipodal 
polar  nucleus,  are  not  formed,  the  endosperm  being  derived  en- 
tirely from  the  micropylar  polar  nucleus.  In  Antennaria  alpi- 
na  Juel  22  found  that  the  polar  nuclei  do  not  fuse,  although  they 
behave  normally  in  A.  dioica,  as  the  same  investigator  35  has 


THE  ENDOSPERM 


167 


a- 


observed.  In  Lemna  Caldwell 24  states  that  often  the  polar 
nuclei  do  not  fuse,  in  which  case  he  observed  that  the  micro- 
pylar  polar  produced  some  free  endosperm  nuclei,  and  probably 
the  antipodal  one  also.  In  Limnocharis,  one  of  the  Alismaceae, 
there  is  also  no  fusion  (Hall  50),  since  no  antipodal  polar  nucleus 
is  formed,  and  all  the  endosperm,  which  eventually  fills  the  sac, 
is  derived  from  the  micropylar  polar 
nucleus.  In  Casuarina,  according 
to  Treub,12  there  are  no  antipodals 
or  polar  nuclei,  and  the  endosperm 
is  formed  before  fertilization  and 
independently  of  any  fusion  (Fig. 
67,  B).  It  should  be  stated,  how- 
ever, that  in  a  recent  study  of  Casu- 
aruta  by  Frye 59  abundant  endo- 
sperm was  found  before  the  first 
division  of  the  egg,  but  probably 
not  before  fertilization.  For  exam- 
ple, the  same  investigator  56  found 
in  Asclepias  sixteen  and  thirty-two 
endosperm  nuclei  before  the  first 
division  of  the  egg,  but  not  before 
fertilization  (Fig.  75).  In  Piper 
and  Heckeria  the  development  of 
endosperm  before  the  first  division 
of  the  fertilized  egg  is  even  more 
extensive.  Johnson 55  represents 
twenty-two  endosperm  cells  in  a 
single  section  of  Piper  (Fig.  76) 

1,1  i  j  •    •  i     i       FIG.  75. — Asclepias  Cornuti.    Large 

and  the  egg  has  not  yet  divided. 
Xot  a  little  confusion  has  arisen 
by  assuming  that  fertilization  and 
the  first  division  of  the  egg  are 
practically  simultaneous.  In  any  event,  the  formation  of  endo- 
sperm without  antecedent  fusion  is  clear  enough  in  some  cases, 
and  indicates  that  while  fusion  usually  serves  to  stimulate 
growth  and  cell  division  it  is  not  an  absolute  prerequisite.  In 
certain  orchids  Xawaschin  36  states  that  the  polar  nuclei  do  not 
fuse,  but  in  this  case  no  endosperm  is  formed. 

In  this  connection  the  experiments  of  Shibata  57  on  Mono- 
12 


O   ** 


development  of  endosperm  before 
division  of  fertilized  egg :  a,  an- 
tipodals ;  e,  egg ;  «,  synergids ;  x 
750.— After  FRYE.W 


-em 


FIG.  76. — A,  Piper  medium,  showing  extensive  development  of  endosperm  before  first, 
division  of  fertilized  egg ;  x  175 ;  B-D.  Peperomia  pellucida :  B,  longitudinal  section 
of  ripe  seed,  showing  the  small  embryo,  scanty  endosperm,  and  abundant  perisperm ; 
x  55 ;  C,  terminal  portion  of  a  similar  section  at  an  early  stage  of  germination ; . 
x  175 ;  D,  longitudinal  section  of  a  germinating  seed,  showing  the  endosperm  pro- 
truding with  the  embryo;  x,55:  o,  antipodals;  c,  cotyledons;  cp,  carpellary  tissue  j. 
0,  endosperm ;  em,  embryo ;  i,  integument ;  o,  oosphere ;  p,  perisperm ;  r,  rhizoid ;  «,, 
synergid ;  st,  stigma ;  t,  tapetal  cells. — After  JOHNSON." 
168 


THE  ENDOSPERM 


169 


tropa  uni  flora  are  of  interest.  In  this  case  the  polar  nuclei  may 
fuse  in  the  absence  of  pollination,  but  the  fusion  may  be  hastened 
or  regulated  by  pollination.  In  normal  cases  fusion  of  polar 
nuclei  occurs  about  five  days  after  pollination,  but  when  pollina- 
tion is  prevented  the  interval  may  be  prolonged  to  ten  days  or 
even  longer.  Development  of  the  endosperm  was  also  induced 
experimentally  in  the  absence  of  fertilization.  When  pollination 
is  prevented,  many  of  the  ovules  die  within  two  or  three  weeks, 
but  in  others  the  sac  enlarges  and  becomes  filled  with  endosperm. 
This  development  of  en- 
dosperm was  observed  in 
from  three  to  five  per  cent 
of  the  ovules,  but  at  a  tem- 
perature of  28°  C.,  or  by 
using  osmotic  solutions,  en- 
dosperm was  developed  by 
from  six  to  twelve  per  cent 
of  the  seeds. 

If  a  fusion  nucleus  is 
formed,  as  is  certainly  gen- 
erally the  case,  it  usually 
begins  to  divide  before  the 
fertilized  egg  and  with 
much  greater  rapidity. 
After  fertilization,  the  egg 
usually  seems  to  rest  for  a 
period  while  free  endo- 
sperm nuclei  are  being 
formed.  For  example, 
among  the  Ranunculaceae 
(Guignard43)  and  in  As- 
clepias  (Frye56)  free  en- 
dosperm nuclei  are  scattered  through  the  sac  before  the  egg 
divides.  But  there  is  every  gradation  from  an  approximately 
simultaneous  division  of  primary  endosperm  nucleus  and  fer- 
tilized egg,  as  usually  in  Sagittaria  (Schaffner 18),  Lilium 
(Coulter  19),  Nelumbo  (Ljon  45),  Sarcodes  (Oliver  "),  Senecio 
(Mottier15),  and  Erigeron  (Land32)  (Fig.  77),  in  which  last 
case  sometimes  the  egg  and  sometimes  the  primary  endosperm 
nucleus  divides  first,  to  a  sac  almost  or  even  completely  filled  with 


FIG.  *11— Erigeron  philadelphicus.  Longitudinal 
sections  of  embryo-sac  after  fertilization.  J, 
fertilized  egg  dividing  before  primary  endo- 
sperm nucleus;  JB,  primary  endosperm  nu- 
cleus dividing  before  egg;  x  550. —  After 

LAND.33 


170  MORPHOLOGY  OF  ANGIOSPERMS 

endosperm  before  the  fertilized  egg  segments,  as  in  Gonyanthes 
Candida  (Treub7),  HecJceria  (Johnson55),  the  Stylidaceae 
(Burns28),  and  Aphyllon  uniflorum  (Smith46).  Even  though 
the  primary  endosperm  nucleus  and  the  fertilized  egg  divide 
simultaneously,  the  much  more  rapid  divisions  of  the  former 
result  in  numerous  free  endosperm  nuclei  before  the  first  few 
segmentations  of  the  egg  have  been  completed. 

In  the  cases  just  cited,  in  which  the  segmentation  of  the 
primary  endosperm  nucleus  precedes  that  of  the  fertilized  egg, 
the  division  does  not  begin  until  after  fertilization,  and  proba- 
bly this  is  true  in  the  majority  of  plants.  As  a  consequence, 
the  impression  is  current  that  the  act  of  fertilization  is  an 
essential  stimulus  to  the  division  of  tthe  primary  endosperm 
nucleus ;  and  there  seems  to  be  no  clear  evidence  to  the  contrary 
when  fertilization  occurs,  unless  it  be  the  case  of  Ranunculus, 
as  reported  by  Coulter,20  in  which  free  endosperm  nuclei  were 
sometimes  observed  scattered  through  the  embryo-sac  before  the 
entrance  of  the  pollen-tube.  To  this  same  category  belong  those 
cases  of  habitual  failure  of  fertilization  in  which  endosperm 
formation  may  occur,  as  in  the  Balanophoraceae,  Antennaria 
alpina  ( Juel  22),  Thalictrum  purpurascens  (Overton51),  Eicli- 
hornia  crassipes  (Smith21),  etc.  It  seems  to  be  very  rare  for 
the  fertilized  egg  to  divide  before  the  primary  endosperm  nu- 
cleus, but  in  Naias  major,  in  which  triple  fusion  occurs,  Guig- 
nard  42  has  observed  that  the  fertilized  egg  divides  immediately, 
and  has  figured  a  two-celled  embryo  by  the  side  of  a  primary 
endosperm  nucleus  in  the  spirem  stage.  It  is  important  to 
note  also  that  in  this  same  species  Guignard  observed  that  the 
male  nucleus  may  fuse  with  the  persistent  synergid  instead  of 
with  the  primary  endosperm  nucleus,  in  which  case  there  is  no 
endosperm,  but  a  second  embryo  (Fig.  103).  Many  cases  of  two 
embryos  lying  side  by  side  with  an  "  unfertilized  "  primary 
endosperm  nucleus  between  them  were  observed.  Recently 
Wylie  60  has  observed  that  in  Elodea  also  the  fertilized  egg 
divides  before  the  primary  endosperm  nucleus. 

It  is  evident  that  the  beginning  of  endosperm  formation    • 
does  not  depend  absolutely  upon   any  of  the  causes  usually 
assigned ;  and  that  while  it  is  in  general  approximately  coinci- 
dent with  the  segmentation  of  the  fertilized  egg,  this  is  merely 
a  coincidence,  for  it  may  be  independent  of  fertilization  and 


THE  ENDOSPERM  171 

even  of  fusion.  Ordinarily  it  must  be  dependent  upon  polar 
fusion,  and  in  some  cases  upon  triple  fusion,  as  indicated  by 
the  behavior  in  Xaias  cited  above;  but  in  the  failure  of  these, 
other  conditions  may  cause  nuclear  division  and  the  formation 
of  endosperm. 

While  in  the  majority  of  plants  the  endosperm  may  be  re- 
garded as  fully  developed,  either  to  remain  as  a  permanent 
tissue  of  the  seed  or  to  be  more  or  less  resorbed  by  the  growing 
embryo,  there  are  certain  plants  in  which  it  is  abortive  or  even 
suppressed.  It  consists  of  only  a  few  scattered  nuclei,  or  at 
most  of  a  parietal  layer  of  free  nuclei,  in  Xaiadaceae,  most  Alis- 
maceae,  Juncagineae,  and  Hydrocharitaceae,  all  of  which  belong 
to  the  Helobiales  among  Monocotyledons.  The  tendency  of  the 
endosperm  to  become  abortive  in  this  particular  alliance  is  evi- 
dently very  strong,  although,  as  Hall50  has  shown  in  Limno- 
charis,  the  endosperm  may  finally  develop  and  become  packed 
about  the  embryo.  With  the  exception  of  the  Helobiales,  disap- 
pearance of  the  endosperm  seems  to  be  very  rare,  having  been 
reported  in  Tropaeolum  and  Trapa\  and  among  the  Orchida- 
ceae  the  endosperm  seems  to  be  entirely  suppressed,  the  polar 
nuclei,  as  a  rule,  neither  fusing  nor  dividing. 

Humphrey  17  has  called  attention  to  what  he  calls  a  pro- 
gressive series  in  the  development  of  the  endosperm  among  the 
Scitamineae,  but  which  seems  to  be  best  interpreted  as  a  retro- 
gressive series.  In  the  Musaceae  an  abundant  starch-bearing 
endosperm  either  fills  the  sac  (Heliconia)  or  nearly  so  (Stre- 
litzia),  the  peripheral  cells  often  forming  an  aleurone  layer; 
in  Zingiberaceae  (Costus)  the  endosperm  is  several  layers  thick 
in  the  lower  part  of  the  sac  and  only  aleurone-bearing ;  in  Can- 
naceae  (C.  indica)  the  endosperm  is  a  single  aleurone-bearing 
layer  lining  the  sac ;  while  in  Marantaceae  (Thalia  dealbata) 
the  endosperm  is  probably  not  represented  at  all  in  the  mature 
seed. 

Strasburger  4  has  called  attention  to  the  two  general  meth- 
ods of  endosperm  formation  among  Angiosperms.  .In  the  ma- 
jority of  plants  observed  it  begins  with  free  nuclear  division; 
but  in  many  cases,  chiefly  among  Dicotyledons,  the  first  division 
of  the  primary  endosperm  nucleus  is  accompanied  by  a  wall 
dividing  the  sac  into  two  chambers  (Fig.  74).  While  these 
two  methods  of  initiating  endosperm  formation  are  quite  dif- 


172  MORPHOLOGY  OF  ANGIOSPERMS 

ferent,  the  subsequent  stages  of  endosperm  development  result 
in  all  kinds  of  intergrading  conditions,  as  will  be  shown  later. 
Even  when  the  endosperm  begins  with  free  nuclear  division, 
a  rudimentary  plate  often  appears,  suggesting  derivation  from, 
an  endosperm  in  which  nuclear  division  was  followed  by  cell- 
formation. 

The  history  of  the  development  of  endosperm  initiated  by 
free  nuclear  division  is  nearly  identical,  in  most  cases,  with 
the  history  of  the  female  gametophyte  in  Gymnosperms,  modi- 
fied, of  course,  by  the  presence  of  a  developing  embryo.  It  is 
an  interesting  fact,  also,  that  the  early  stages  in  the  develop- 
ment of  the  endosperm  bear  a  striking  resemblance  to  early 
stages  in  the  development  of  the  embryo  of  Cycadales  and  some 
other  Gymnosperms.  There  is  the  same  simultaneous  nuclear 
division,  often  the  parietal  placing,  and  later  the  appearance  of 
cell  walls. 

The  primary  endosperm  nucleus,  usually  in  contact  with 
the  egg,  or  nearly  so,  divides,  and  subsequent  divisions  follow 
with  great  rapidity,  Guignard  41  remarking  that  in  Zea  he  was 
unable  to  follow  the  course  of  division,  and  other  observers  call- 
ing attention  not  only  to  the  great  rapidity  with  which  one  set 
of  divisions  is  followed  by  another,  but  also  to  their  simultane- 
ous character.  A  common  form  of  statement  is  that  at  first  the 
free  nuclei  remain  for  a  time  in  the  vicinity  of  the  egg,  but 
sooner  OT  later  migrate  in  every  direction  toward  the  wall  of 
the  embryo-sac,  where  they  become  equally  distributed  and 
embedded  in  a  lining  cytoplasmic  layer.  The  real  fact,  how- 
ever, is  that  this  apparent  movement  of  the  nuclei  is  due  to  the 
rapid  enlargement  of  the  sac,  the  cytoplasm  becoming  more  and 
more  vacuolate  and  finally  occurring  chiefly  as  a  wall  layer. 
By  this  increasing  vacuolation  the  nuclei  are  naturally  driven 
to  the  wall.  In  this  parietal  position  free  nuclear  division  con- 
tinues, until  finally  walls  are  formed  and  a  layer  of  parietal 
cells  is  organized. 

These  first  walls  usually  "  cut  out "  only  one  nucleus  in 
each  cell,  but  in  some  cases  (Corydalis  cava,  Staphylea  pinnata, 
Armeria  vulgaris,  etc.)  Strasburger  4  noted  that  two  to  four 
nuclei  might  be  enclosed  by  a  cell  wall,  but  that  they  afterward 
fuse  to  form  a  single  nucleus  (Fig.  78).  Tischler 39  has 
recently  reexamined  Corydalis  cava  and  states  that  when  septa 


THE  ENDOSPERM 


173 


appear  many  nuclei  are  always  enclosed  in  each  cell  and  sub- 
sequently fuse.     In  this  particular  case  the  free  nuclear  divi-  , 
sions  are  often  irregular,  and  of  course  the  number  of  chromo- 
somes is  exceedingly  variable,  a  fact  very  common  in  all  endo- 


FIG.  7S. — Advanced  stages  in  development  of  endosperm.  A,  Reseda,  odorata,  upper 
part  of  figure  showing  free  nuclear  division,  while  in  lower  part  nuclear  division  is 
accompanied  by  formation  of  cell  walls ;  x  860 ;  B,  Caltha  palustris,  showing  all 
nuclear  divisions  accompanied  by  formation  of  walls,  x  155;  (7,  CorydaUs  cava. 
showing  free  nuclear  division  within  cells  of  endosperm;  D,  the  same,  showing 
multinucleate  endosperm ;  x  860. — After  STRASBURGZR.* 

sperm.  The  same  phenomenon  was  observed  by  Humphrey17 
in  Canna  indica,  in  which  the  parietal  layer  of  free  nuclei 
becomes  blocked  out  by  walls,  each  "  block  "  containing  several 


1T4  MORPHOLOGY  OF  ANGIOSPERMS 

nuclei  that  apparently  fuse  into  one.  The  irregular  and  usu- 
ally large  number  of  chromosomes  found  in  the  nuclei  of  endo- 
sperm tissue  is  doubtless  due  to  "  double  fertilization "  and 
other  nuclear  fusions. 

The  parietal  plate  of  cells  by  division  gradually  encroaches- 
upon  the  general  cavity  of  the  embryo-sac,  either  filling  it  up 
compactly  about  the  embryo,  or  leaving  more  or  less  of  a  cavity 
containing  cell  sap,  which  in  the  coconut  becomes  of  extraordi- 
nary size. 

In  many  cases  a  fully  developed  endosperm  is  more  or  less 
displaced  by  the  growing  embryo,  so  that  in  the  mature  seed  it 
may  be  much  reduced  or  even  obliterated.  Among  the  Mono- 
cotyledons the  embryo  of  the  Gramineae  is  at  first  completely 
invested  by  endosperm,  but  becomes  eccentric  by  displacing  it 
on  one  side;  and  the  embryo  in  some  Araceae  finally  replaces 
all  the  endosperm;  but  for  the  most  part  the  Monocotyledons 
are  characterized  by  retaining  the  endosperm  in  the  mature 
seed.  Among  the  Dicotyledons,  however,  it  is  characteristic  of 
certain  families,  among  the  important  ones  being  Cupuliferae, 
Leguminosae,  Cucurbitaceae,  and  Compositae,  for  the  embryo 
to  have  entirely  displaced  the  endosperm  at  the  maturity  of  the 
seed,  the  gain  in  size  being  almost  entirely  in  the  cotyledons. 
It  must  not  be  supposed  that  in  all  cases  the  formation  of  endo- 
sperm continues  from  the  first  free  nuclear  division  to  a  tissue 
filling  the  embryo-sac.  Illustrations  could  be  introduced  show- 
ing a  cessation  of  endosperm  formation  at  every  stage.  It  may 
stop  with  a  few  free  nuclei,  or  with  the  parietal  placing  of  free 
nuclei,  or  with  a  parietal  plate  of  tissue.  An  interesting  case 
is  that  of  Tricyrtis  (Liliaceae),  recently  described  by  Ikeda,54 
in  which  free  endosperm  nuclei  are  distributed  through  a  sac 
full  of  cytoplasm,  and  assume  very  irregular  and  bizarre  forms, 
the  parietal  position  never  being  assumed. 

The  second  general  method  of  endosperm  formation — 
namely,  that  in  which  the  first  division  of  the  primary  endo- 
sperm nucleus  is  accompanied  by  a  wall  dividing  the  sac  into 
two  chambers — is  found  chiefly  among  Dicotyledons,  and  among 
them  it  is  especially  characteristic  of  saprophytic  and  parasitic 
forms,  Cuscuta  being  a  marked  exception  in  that  its  endosperm 
begins  with  free  nuclear  division.  Usually  the  wall  divides  the 
sac  into  two  approximately  equal  chambers,,  but  naturally  the 


THE  ENDOSPERM 


175 


relative  size  of  the  chambers  depends  upon  the  position  of  the 
dividing  nucleus  (Fig.  74). 

Among  Monocotyledons,  the  endosperm  of  Sagittaria 
(Schaffner  18)  develops  rapidly  in  the  micropylar  chamber 
into  a  walled  tissue,  the  endosperm  nucleus  of  the  antipodal 
chamber  enlarging  much  but  not  dividing  for  a  long  time,  when 
two  or  three  nuclei  may  be  formed,  all  of  them  increasing 
greatly  (Fig.  79).  Practically  the  same  thing  occurs  in  Limno- 
charis  (Hall50),  but  the  nucleus  of  the  antipodal  chamber  en- 
larges without  dividing.  In  Ruppia  rostellata  (Murbeck58)  a 


B 


FIG.  79. — Sagittaria  variabilis.  A,  two  nuclei  of  endosperm  separated  by  wall :  a,  an- 
tipodals,  x  200 ;  B,  compact  endosperm  tissue  developed  from  upper  cell,  the  lower 
merely  growing  large  without  dividing;  x  108. — After  SCHAFFNEK.IB 

wall  is  formed  at  the  first  division  of  the  endosperm  nucleus,  the 
antipodal  chamber  remaining  small  and  with  undividing  nucleus, 
but  a  large  number  of  free  nuclei  being  formed  in  the  micro- 


176  MORPHOLOGY  OF  ANGIOSPERMS  ' 

pylar  chamber.  In  Potamogeton  (Holferty  44)  the  endosperm 
is  developed  only  as  a  parietal  layer  of  free  nuclei;  but  all  of 
these  seem  to  have  come  from  the  micropylar  endosperm-cell 
of  the  first  division,  the  lower  one  becoming  very  large  but  not 
dividing,  a  tendency  similar  to  that  in  Sagittaria  and  Limno- 
charis,  but  without  the  formation  of  a  transverse  wall  in  the  sac. 

Among  the  Dicotyledons  instances  of  a  chambered  embryo- 
sac  are  numerous.  Hofmeister  1  has  given  a  long  list  of  them, 
and  these, with  others  added  since,  are  approximately  as  follows: 
Among  the  Archichlamydeae  they  are  the  Saururaceae,  Loran- 
thaceae,  Balanophoraceae,  Santalaceae,  Aristolochiaceae,  Nym- 
phaeaceae,  Ceratophyllaceae,  Loasaceae,  a  list  composed  in  the 
main  of  primitive  or  saprophytic  and  parasitic  forms.  In  fact, 
the  chambered  sac  is  distinctly  lacking  in  the  more  important 
and  characteristic  groups  of  the  Archichlamydeae.  Among  the 
Sympetalae,  chambered  sacs  occur  in  the  Pyrolaceae,  Mono- 
tropaceae,  Vacciniaceae,  Hydrophyllaceae  (Nemophila),  Sola- 
naceae,  Verbenaceae,  Selaginaceae,  Labiatae,  Scrophulariaceae, 
Orobanchaceae,  Bignoniaceae,  Pedaliaceae,  Acanthaceae,  Plan- 
taginaceae,  and  Campanulaceae.  Although  most  largely  repre- 
sented among  Sympetalae,  it  will  be  noted  that  chambered 
sacs  occur  chiefly  in  saprophytic  or  parasitic  forms,  and  among 
the  Personales.  The  phenomenon  seems  thus  to  be  associated 
with  peculiar  conditions  of  nutrition  or  a  certain  configuration 
of  the  embryo-sac. 

In  the  case  of  two-chambered  sacs  among  Dicotyledons,  it 
does  not  seem  to  be  common  for  endosperm  to  form  in  both 
chambers,  although  this  is  reported  to  be  the  case  in  Balano- 
phoraceae, Aristolochiaceae,  Pyrolaceae,  and  Monotropaceae. 
In  the  majority  of  cases  the  endosperm  develops  only  in  the 
micropylar  chamber,  in  connection  with  the  embryo,  as  in  Sau- 
ruraceae, Viscum  (Loranthaceae),  Santalaceae,  Xymphaeaceae, 
Globularia  (Selaginaceae),  Scrophulariaceae,  and  Orobancha- 
ceae. In  Saururus  (Johnson34)  the  embryo-sac  is  flask-shaped, 
the  wall  cutting  off  the  neck  from  the  large  venter,  and  the  en- 
dosperm developing  only  in  the  former.  In  Nymphaea  and 
Nuphar  (Cook52)  the  endosperm  develops  only  in  the  micro- 
pylar chamber,  while  the  antipodal  chamber  extends  as  an  haus- 
torial  tube  to  the  chalazal  extremity  of  the  ovule.  It  is  of  interest 
to  note  that  until  Cook's  work  the  endosperm  of  these  genera  was 


v 


THE  ENDOSPERM 


177 


said  to  begin  with  free  nuclear  division,  followed  by  a  wall  cut- 
ting off  the  micropylar  end  of  the  sac ;  and  the  same  statement 
in  reference  to  Ceratophyllum  has  been  disproved  recently  by 
Strasburger.49  The  endosperm  is  said  to  develop  only  in  the 
antipodal  chamber  in  Loranthus,  Vacciniaceae,  Verbenaceae, 
Hebenstreitia  (Selaginaceae),  Bignoniaceae,  and  Acanthaceae. 
In  Trapella  (Oliver10),  a  genus  of  the  Pedaliaceae,  although 
the  sac  is  not  chambered  by  a  wall, 'the  endosperm  develops  only 
in  the  lower  two-thirds,  a  sort  of  diaphragm  of  thick-walled  en- 
dosperm-cells cutting  off  the  broad  micropylar  end  of  the  sac. 


B 


FIG.  80. — Ceratophyllum  submersum.  Development  of  endosperm  and  embryo.  A,  first 
division  of  embryo,  six  cells  in  endosperm;  x  250;  B,  embryo  and  endosperm  more 
advanced ;  x  250 ;  .C-D,  entire  embryo  seen  from  opposite  sides,  C  showing  the  two 
cotyledons  separate  and  D  nearly  united  ;  x  50. — After  STRASBCROER.49 

Cases  are  also  known  in  which  more  than  two  chambers  are 
formed  in  the  embryo-sac  and  followed  by  ordinary  cell-forma- 
tion. For  example,  in  Ceratophyllum  (Strasburger49)  at  the 
first  division  of  the  primary  endosperm  nucleus  the  sac  is 
divided  into  two  approximately  equal  chambers.  The  nucleus 
in  the  antipodal  chamber  does  not  divide  again,  but  at  the  next 
division  in  the  micropylar  chamber  another  wall  across  the  sac 


178  MORPHOLOGY  OF  ANGIOSPERMS 

is  formed,  so  that  there  are  three  superposed  chambers,  and  only 
in  the  one  nearest  the  micropyle  does  division  proceed.  As  a 
result,  a  dense,  small-celled  tissue  is  formed  near  the  embryo 
(Fig.  80).  In  Datura  laevis  (Guignard  48),  after  the  first  divi- 
sion into  two  chambers  (Fig.  74),  transverse  walls  are  formed 
in  each,  resulting  in  four  superposed  chambers  in  which  further 
division  proceeds  in  various  planes. 

V  There  are  also  cases  in  which  each  division  of  an  endosperm 
nucleus  is  accompanied  by  a  transverse  wall  across  the  sac,  as 
in  Sar codes  (Oliver11),  in  which  the  mature  sac  is  several- 
chambered  by  a  series  of  delicate  transverse  walls.  The  same  is 
doubtless  true  of  Pistia,  whose  narrow  sag  contains  a  row  of 
broad  discoid  endosperm-cells  that  lie  like  transverse  chambers. 
One  of  the  most  exceptional  cases  of  wall-formation,  however^ 
is  that  of  Peperomia  pellucida  (Johnson31),  in  which  the  first 
division  of  the  very  large  primary  endosperm  nucleus,  formed 
by  the  fusion  of  eight  nuclei,  is  followed  by  a  wall  from  the 
fertilized  egg  to  the  base  of  the  sac,  further  divisions  following 
until  the  sac  is  packed  with  forty  or  more  endosperm-cells.  In 
a  recent  study  of  Heckeria  also,  one  of  the  Piperaceae,  the 
same  investigator  55  has  found  the  same  general  condition  as  in 
Peperomia,  in  that  the  endosperm  is  "  cellular  "  from  the  first, 
filling  the  sac  before  the  egg  divides.  It  is  worthy  of  note  that 
the  endosperm  of  Piper  (Johnson  55),  on  the  other  hand,  begins 
with  free  nuclear  division.  It  is  evident  from  these  differences 
in  closely  related  genera,  also  noted  by  Hofmeister  2  and  Hegel- 
maier,8  that  methods  of  endosperm  formation  can  not  indicate 
relationship. 

The  mature  and  permanent  endosperm  is  a  tissue  with  no 
intercellular  spaces,  w;hose  cells  are  either  thin-wralled,  form- 
ing an  endosperm  of  delicate  texture,  or  thick-walled,  resulting 
in  a  horny  endosperm,  as  in  palms,  umbellifers,  etc.  In  case  the 
thickening  of  the  walls  becomes  excessive,  the  endosperm  is 
stony,  as  in  Phytelephas,  the  palm  whose  seeds  furnish  the 
so-called  "  vegetable  ivory." 

The  endosperm  has  sometimes  been  observed  to  continue  its 
growth  after  it  has  filled  the  sac.  Hofmeister  describes  the  en- 
dosperm of  Crinum  capense  and  some  other  Amaryllidaceae  as 
bursting  the  seed-coats,  and  even  the  ovary  wall,  the  cells  devel- 
oping chlorophyll,  and  the  tissue  remaining  succulent  and  form- 


THE  ENDOSPERM  179 

ing  intercellular  spaces.  A  similar  extensive  growth,  and 
escape  of  the  endosperm  is  reported  to  occur  during  the  germi- 
nation of  the  seeds  of  Ricinus.  In  the  germination  of  the  seeds 
of  certain  Piperaceae  (Peperomia  and  Heckeria)  Johnson  53>  55 
has  described  the  endosperm  as  bursting  out  of  the  seed-coat, 
and  continuing  to  jacket  the  embryo,  which  at  germination  is  a 
globular  undifferentiated  mass  of  cells,  until  the  root,  hypocotyl, 
and  cotyledons  are  organized.  In  the  same  papers  Johnson  calls 
attention  to  the  fact  that  the  endosperm  of  these  Piperaceae 
is  not  a  storage  region,  but  digests,  absorbs,  and  passes  on  food 
material  to  the  embryo  from  the  much,  more  abundant  peri- 
sperm,  which  is  the  real  storage  tissue.  This  restriction  of  the 
function  of  the  endosperm  Johnson  S4  had  already  pointed  out 
in  Saururus,  and  suggests  the  probability  that  this  same  relation 
between  endosperm  and  perisperm  obtains  in  all  seeds  with 
abundant  perisperm  as  in  Polygonaceae,  Chenopodiaceae,  Phy- 
tolaccaceae,  Caryophyllaceae,  etc.  The  following  quotation 55 
will  serve  to  make  plain  the  author's  point  of  view : 

"  Observations  thus  far  made  lead  me  to  believe  that  in  the  peri- 
sperm-containing  seeds  mentioned  the  embryo  sporophyte  of  the  second 
generation  is  never  nourished  by  the  parent  sporophyte  directly,  but 
always  through  the  intermediate  gametophyte.  In  general,  then,  we 
find  that  the  food  substance  supplied  to  the  embryo  by  the  nucellus 
may  pass  through  the  endosperm  and  be  stored  in  the  embryo  during 
the  ripening  of  the  seed,  as  in  Cucurbita  and  Phaseolus  ;  or,  secondly, 
the  food  may  be  stopped  in  transit  between  the  nucellus  and  the  embryo 
and  stored  in  the  endosperm,  there  to  be  held  during  the  resting  period 
of  the  seed  and  delivered  over  to  the  embryo  only  at  the  time  of  sprout- 
ing, as  in  Ricinus,  Zea,  and  apparently  all  Gymnosperms  ;  or,  finally, 
the  food  supply  for  the  developing  embryo  may  be  stored  in  the  nucel- 
lus itself  until  the  time  of  germination,  when  it  is  passed  on  to  the 
embryo  through  the  endosperm,  as  in  Saururus,  Peperomia,  Phyto- 
lacca,  Canna,  and  others." 

The  phenomenon  of  xenia  has  a  direct  bearing  upon  any 
discussion  of  the  endosperm.  The  name  was  applied  by  Focke,5 
in  1881,  to  the  direct  effect  of  pollen  on  seeds  and  fruits  out- 
side of  the  embryo,  as  shown  in  hybrids.  The  case  of  peas  has 
long  been  cited,  but  Giltay  14  has  shown  that  the  effects  referred 
to  occur  in  the  cotyledons,  and  therefore  can  not  be  considered 
as  xenia.  So  far  as  definitely  known,  the  effect  of  foreign 
pollen  outside  of  the  embryo  is  observed  only  in  the  endosperm, 


180  MORPHOLOGY  OF  ANGIOSPERMS 

as  first  pointed  out  by  Kornicke,3  and  this  has  been  most  clearly 
established  in  the  crossing  of  races  of  corn.  It  also  appears 
that  this  influence  of  foreign  pollen  extends-  only  to  the  color 
of  the  endosperm  and, the  chemical  composition  of  the  reserve 
materials,  the  size  and  form  of  the  kernels  remaining  un- 
changed, as  stated  by  Correns.25  For  example,  if  white  or  yel- 
low corn  be  crossed  with  pollen  from  a  red  corn,  many  of  the 
resulting  kernels  will  be  red  or  variously  mottled ;  or  if  sweet 
corn,  with  its  wrinkled  and  sugary  endosperm,  be  crossed  with 
pollen  from  dent  or  flint  corn,  the  result  is  smooth  kernels  with 
starchy  endosperm. 

The  possibility  of  such  a  direct  effect  of  pollen  was  for  a 
long  time  questioned,  and  the  phenomenon  remained  inexpli- 
cable. With  the  discovery  of  "  double  fertilization  "  or  triple 
fusion  by  Nawaschin  23  in  1898,  the  explanation  of  xenia  oc- 
curred simultaneously  and  independently  to  Correns,25  De 
Vries,27  and  Webber,40  the  paper  of  the  last  investigator  being 
a  very  complete  resume  and  discussion  of  the  subject  based  upon 
his  own  extensive  experimental  work.  To  claim  that  the  phe- 
nomenon of  xenia,  as  observed  in  corn,  is  due  to  the  fusion  of 
one  of  the  male  nuclei  with  the  primary  endosperm  nucleus  was 
an  assumption,  although  an  irresistible  one,  until  such  fusion 
was  demonstrated  by  Guignard  41  in  1901.  It  has  been  proved 
repeatedly  that  when  xenia  occurs  the  embryo  is  a  hybrid,  so 
that  we  have  in  xenia  not  only  a  hybrid  endosperm,  but  a  gross 
demonstration  of  the  occurrence  and  effect  of  the  triple  fusion, 
and  also  an  indication  of  the  sort  of  characters  that  can  be 
brought  into  a  structure  by  a  male  nucleus. 

•  In  many  cases  of  xenia  following  the  crossing  of  races  of 
different  colors,  the  kernels  are  not  of  uniform  color,  but  are 
parti-colored  or  variously  mottled.  The  ingenious  explanation 
suggested  by  Webber  is  that  the  male  nucleus  has  failed  to  unite 
with  the  fusion-nucleus  and  may  be  able  to  divide  independ- 
ently. If  so,  there  would  result  two  cell-races  of  different 
characters  that  might  be  variously  arranged  with  reference  to 
one  another  in  the  endosperm.  It  is  entirely  conceivable  that 
under  favorable  conditions  of  nutrition  and  physical  environ- 
ment an  independent  male  nucleus  may  begin  divisions,  espe- 
cially as  this  has  been  observed  in  the  case  of  certain  animals ; 
but  it  seems  more  probable  that  the  independent  appearance  of 


THE  ENDOSPERM  181 

these  racial  characters  is  due  to  the  incompleteness  of  the  triple 
fusion,  since  it  is  well  known  that  division  of  the  primary  endo- 
sperm nucleus  often  begins  before  the  constituent  nuclei  have 
k*t  their  identity.  In  fact,  Webber  calls  attention  to  the  begin- 
ning of  division  before  complete  fusion  in  the  case  of  the  eggs 
of  certain  animals,  and  the  same  is  true  of  the  sexual  fusion- 
nucleus  of  some  Gymnosperms.  An  alternative  hypothesis  sug- 
gested by  Webber  is  that  the  male  nucleus  may  fuse  with  one  of 
the  polar  nuclei,  the  other  remaining  independent  and  dividing. 
These  hypotheses  are  valuable  in  suggesting  investigation  as  to 
whether  the  male  nucleus  ever  divides  independently  in  the  em- 
bryo-sac, or  whether  it  may  unite  with  one  polar  nucleus,  the 
other  dividing  independently. 

It  remains  to  consider  the  morphological  character  of  the 
endosperm  of  Angiosperms.  In  view  of  the  details  as  to  its 
origin  and  behavior  given  above,  it  is  evident  that  it  is  a  struc- 
ture peculiarly  difficult  to  interpret.  The  view  has  long  been 
held,  dating  from  Hofmeister,  that  the  endosperm  is  belated 
vegetative  tissue  of  the  female  gametophyte,  stimulated  in  a 
general  way  to  develop  by  the  act  of  fertilization,  and  in  every 
way  the  morphological  equivalent  of  the  structure  bearing  the 
same  name  among  Gymnosperms.  Strasburger  37  has  suggested 
that  this  postponement  of  the  formation  of  endosperm  is  of 
advantage  in  avoiding  the  waste  that  would  follow  its  formation 
and  separation  from  the  parent  plant  with  every  unfertilized 
ovule.  Of  course  the  serious  difficulty  in  this  view  of  the  nature 
of  the  endosperm  was  that  it  offered  no  historical  explanation 
of  the  fusion  of  the  polar  nuclei.  It  could  only  claim  that 
fusions  of  vegetative  nuclei,  evidently  resulting  in  growth- 
stimulus,  are  by  no  means  unknown.,  and  in  fact  occur  in  the 
endosperm  itself.  This  view  does  not  appear  to  have  been 
seriously  disturbed  by  the  claim  of  Le  Monnier  9  in  1887,  that 
the  fusion  of  the  polar  nuclei  is  a  sexual  process,  and  that  there- 
fore the  endosperm  is  a  second  embryo  modified  to  serve  as 
food  tissue. 

With  the  discovery  of  the  fact  that,  at  least  in  many  cases, 
a  male  nucleus  enters  into  the  organization  of  the  primary  endo- 
sperm nucleus,  the  old  view  has  been  seriously  menaced.  The 
commonly  used  phrases  "  double  fertilization "  and  "  double 
fecundation "  indicate  general  consent  to  the  view  that  this 


182  MORPHOLOGY  OF  ANGIOSPERMS 

act  of  the  male  nucleus  is  a  case  of  true  fertilization,  the  infer- 
ence being  that  the  endosperm  is  a  second  embryo  or  sporophyte, 
as  Le  Monnier  had  suggested. 

Strasburger  37  in  discussing  the  whole  subject  concludes  that 
the  triple  fusion  is  not  real  fertilization.  Of  course  in  such  a 
discussion  much  depends  upon  the  definition  of  fertilization. 
Strasburger  distinguishes  between  "  generative  fertilization " 
and  "  vegetative  fertilization/'  the  former  being  a  definite 
union  of  parental  qualities  and  resulting  in  an  embryo,  the 
latter  a  fusion  resulting  merely  in  a  growth-stimulus.  He 
thinks  that  the  endosperm  is  historically  a  gametophyte,  and 
that  the  fusion  which  initiates  it  has  no  origin  in  an  act  of 
fertilization. 

Later,  Miss  Sargant  38  published  an  admirable  resume  of 
the  subject,  together  with  a  clear  statement  of  the  problems 
involved  and  certain  suggestions  by  way  of  interpretation.  She 
very  justly  states  that  if  the  endosperm  "  arose  from  a  belated 
formation  of  prothallus,  we  must  trace  the  origin  of  the  triple 
nuclear  fusion  which  precedes  its  development " ;  and  if  it  is 
a  modified  embryo  "  we  have  to  account  for  the  interference  of 
the  lower  polar  nucleus  with  the  act  of  fertilization,  and  for 
the  subsequent  development  of  a  body  unlike  a  normal  embryo." 
Her  suggested  interpretation  of  the  phenomenon  is  that  the 
fusion  of  the  male  nucleus  with  the  micropylar  polar  nucleus,  an 
undoubted  female  nucleus,  both  containing  the  reduced  number 
of  chromosomes,  is  a  typical  sexual  union;  but  that  the  antip- 
odal polar  nucleus,  with  its  vegetative  character,  and  indefi- 
nite and  usually  increased  number  of  chromosomes,  is  a  disturb- 
ing factor,  and  the  result  is  not  a  normal  embryo  but  a  small 
and  short-lived  mass  of  tissue.  She  aptly  cites  the  experiments 
of  Boveri 13  with  sea-urchins,  in  forcing  more  than  one  sperm- 
nucleus  to  unite  with  a  single  egg-nucleus  and  producing  mon- 
strous larval  structures.  "  The  presence  of  the  third  nucleus, 
therefore,  with  its  redundant  chromosomes,  serves  to  secure  the 
degeneracy  of  the  resulting  tissue."  This  means,  of  course,  that 
the  endosperm  is  a  degenerate  embryo,  and  that  the  triple 
fusion  is  a  true  sexual  union  whose  normal  result  has  been 
interfered  with  by  the  presence  of  a  non-sexual  nucleus  in  the 
combination. 

It  is  impossible  to  solve  such  a  problem  by  a  discussion  of 


THE  ENDOSPERM  183 

the  data  we  possess.  The  phytogeny  of  the  endosperm  must  be 
traced,  and  the  place  of  the  polar  fusion  and  of  the  triple  fusion 
in  its  history  determined  before  opinions  cease  to  differ  as  to 
its  morphological  character.  In  view  of  such  facts  as  we  have, 
however,  we  are  inclined  to  hold  with  Strasburger  that  the 
endosperm  of  Angiosperms  is  a  gametophytic  structure,  and 
that  the  polar  fusion  and  the  triple  fusion  are  interpolations 
in  its  history  that  do  not  change  its  essential  character.  The 
fact  that  endosperm  sometimes  forms  before  fertilization  indi- 
cates that  the  triple  fusion  is  not  an  essential  prerequisite ;  the 
fact  that  endosperm  forms  without  the  polar  fusion  points  at 
least  to  the  conclusion  that  it  was  once  developed  without  it; 
the  indifference  of  the  male  nucleus  as  to  which  polar  nucleus 
it  fuses  with  (Lilium,  Asclepias)  does  not  show  the  selective 
attraction  connected  with  sex-fusion ;  and  the  further  fact  that 
when  an  undoubted  fertilization  occurs,  whether  of  egg,  of  syn- 
ergid,  or  of  upper  polar  nucleus,  an  embryo  is  the  result,  indi- 
cates that  the  presence  of  the  male  nucleus  in  triple  fusion  is  of 
subsidiary  rather  than  of  dominating  importance.  That  the 
fusing  male  nucleus  does  introduce  parental  characters  that 
manifest  themselves  in  the  endosperm  is  proved  by  the  phenom- 
enon of  xenia,  but  this  does  not  seem  necessarily  to  prove  the 
sporophytic  character  of  the  endosperm.  In  fact,  the  develop- 
ment and  structure  of  the  endosperm  of  Angiosperms  is  so  much 
like  that  of  Gymnosperms  that  it  seems  easier  to  regard  the 
various  fusions  as  merely  resulting  in  a  stimulus  to  growth  than 
to  imagine  a  degenerate  embryo  assuming  this  particular  de- 
velopment and  structure.  Of  course  one  might  go  to  the  ex- 
treme, and  regard  the  endosperm  as  neither  gametophyte  nor 
sporophyte,  but  as  a  composite  tissue  involving  both,  but  this 
hardly  seems  to  be  necessary. 

LITERATURE  CITED 

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der  Phanerogamen.    Jahrb.  Wiss.  Bot.  1 :  82-188.  pis.'  7-10.  1858. 

— .    Neue  Beitrage  zur  Kenntniss  der  Embryobildung    der 

Phaiierogamen.     Abhandl.  Konigl.  Sachs.  GeselL  Wiss.  6:  533- 

672.  pis.  1-27.  1859. 

3.  KORNICKE,  F.    Vorlaufige  Mittheilungen  iiber  den  Mais.    Sitz- 

ungsb.  Niederrh.  G-esell.  Nat.  Heilk.  Bonn.  1872. 

4.  STRASBURGER,  E.    Zellbildung  und  Zelltheilung.  Ed.  3    Jena  1880 

13 


184  MORPHOLOGY  OF  ANGIOSPERMS 

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Ill  and  IV.  Ann.  Jard.  Bot.  Buitenzorg  3:  120-128.  pis.  18-19. 
1883. 

8.  HEGELMAIER,  F.    Untersuchungen  iiber  die  Morphologic  des  Di- 

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9.  LE  MONNIER,  G.     Sur  la  valeur  morphologique  de  1'albumen  chez. 

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Trapella,  a  New  Genus  of  Pedalineae.  Annals  of  Botany  2 :  75- 
115.  pis.  5-9.  1888. 

11.  -      — .     On  Sarcodes  sanguined.    Annals  of  Botany  4 :  303-326. 

pis.  17-21.  1890. 

12.  TREUB,  M.    Sur  les  Casuarinees  et  leur  place  dans  le  systeme  natu- 

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14.  GILTAY,  E.    Ueber  den  directen  Einfluss  des  Pollens  auf  Frucht- 

und  Samenbildung.     Jahrb.  Wiss.  Bot.  25 :  489-509.  pi.  23.  1893. 

15.  MOTTIER,  D.  M.    On  the  Embryo-Sac  and  Embryo  of  Senecio 

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16.  TREUB,  M.    L'organe  femelle  et  1'apogamie  du  Balanophora  elon- 

gata.    Ann.  Jard.  Bot.  Buitenzorg  15:  1-22.  pis.  1-8.  1898. 

17.  HUMPHREY,  J.  E.    The  Development  of  the  Seed  in  Scitamiiieae. 

Annals  of  Botany  10 :  1-40.  pis.  1-4.  1896. 

18.  SCHAFFNER,  J.  H.    Contribution  to  the  Life  History  of  Sagittaria 

variabilis.    Bot.  Gazette  23 :  252-273.  pis.  20-26.  1897. 

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philadelphicum.    Bot.  Gazette  23 :  412-422.  pis.  32-34.  1897. 

20.  .    Contribution  to  the  Life  History  of  Eanunculus.     Bot. 

Gazette  25 :  73-88.  pis.  4-7.  1898. 

21.  SMITH,  E.  W.     A  Contribution  to  the  Life  History  of  the  Poiite- 

deriaceae.     Bot.  Gazette  25 :  324-337.  pis.  19-20.  1898. 

22.  JUEL,  H.  O.     Parthenogenesis  bei  Antennaria  alpina  (L.)  E.  Br. 

Bot.  Centralbl.  74:  369-372.  1898. 

23.  NAWASCHIN,  S.    Eesultate  einer  Ee vision  der  Befruchtungsvor- 

gange  bei  Lilium  Martagon  und  Fritillaria  tenella.  Bull. 
Acad.  Imp.  Sci.  St.  Petersbourg  9:  377-382.  1898;  reviewed  in 
Bot.  Centralbl.  78 :  241-245.  1899. 

24.  CALDWELL,  O.  W.    On  the  Life  History  of  Lemna  minor.    Bot 

Gazette  27:  37-66.  figs.  59.  1899. 

25.  CORRENS,  C.     Untersuchungen  iiber  die  Xenien  bei  Zea  Mays. 

Ber.  Deutsch.  Bot.  Gesell.  17:  410-417.  1899. 


THE  ENDOSPERM  185 

26.  LOTSY,  J.  P.     Balanophora    globosa    Jungh.    Eine    wenigstens 

ortlich-verwittwete  Pflanze.  Ann.  Jard.  Bot.  Buitenzorg  II.  1 : 
174-186.  pis.  26-29.  1899. 

27.  DE  VRIES.  H.    Sur  la  fecondation  hybride  de  Talbumen.     Compt 

Rend.  129:  973-975.  1899. 

28.  BURNS,  G.  P.     Beitrage  zur  Kenntniss  der  Stylidiaceen.    Flora  87  r 

313-354.  pis.  13-14.  1900. 

29.  CAMPBELL,  D.  H.     Studies  on  the  Araceae.    Annals  of  Botany 

14:  1-25.  pis.  1-3.  1900. 

30.  CONRAD,  A.  H.    A  Contribution  to  the  Life  History  of  Quercus. 

Bot.  Gazette  29:  408-418.  pis.  28-29.  1900. 

31.  JOHNSON,  D.  S.     On  the  Endosperm  and  Embryo  of  Peperomia 

pellucida.    Bot.  Gazette  30:  1-11.  pi  1.  1900. 

32.  LAND,  W.  J.  G.    Double  Fertilization  in  Compositae.    Bot.  Gazette 

30:  252-260.  pis.  15-16.  1900. 

33.  CHODAT,    R.,    and    BERNARD,    C.      Sur  le  sac  embryonnaire  de 

YHelosis  guayanensis.  Jour.  Botanique  14:  72-79.  pis.  1-2. 
1900. 

34.  JOHNSON,  D.  S.    On  the  Development  of  Saururus  cernuus  L. 

Bull.  Torr.  Bot.  Club  27:  365-372.  pi.  23.  1900. 

35.  JUEL,  H.  O.     Vergleichende  Untersuchungen  liber  typische  und 

parthenogenetische  Fortpflanzung  bei  der  Gattung  Antennaria. 
Handl.  Svensk.  Vetensk.  Akad.  33 :  no.  5.  pp.  59.  pis.  6.  figs.  5. 
1900 ;  reviewed  in  Bot.  Zeit.  59 :  131.  1901. 

36.  XAWASCHIN,  S.    Ueber   die    Befruchtungsvorgange    bei    einigen 

Dicotyledoneen.  Ber.  Deutsch.  Bot.  Gesell.  18 :  224-230.  pi.  9. 
1900. 

37.  STRASBURGER,   E.      Einige    Bemerkungen    zur    Frage    nach  der 

"  doppelten  Befruchtung "  bei  den  Angiospermen.  Bot.  Zeit. 
58:  293-316.  1900. 

38.  SARGANT,  ETHEL.    Recent  Work  on  the  Results  of  Fertilization  in 

Angiosperms.     Annals  of  Botany  14:  689-712.  1900. 

39.  TISCHLER,  G.     Untersuchungen  iiber  die  Entwicklung  des  Endo- 

sperms und  der  Samenschale  von  Corydalis  cava.  Verhandl. 
Naturhist.-Med.  Ver.  Heidelberg  6 :  351-380.  pis.  2.  1900. 

40.  WEBBER,  H.  J.    Xenia,  or  the  Immediate  Effect  of  Pollen  in 

Maize.  Bulletin  22.  Div.  Veg.  Path,  and  Phys.  U.  S.  Dept. 
Agric.  pp.  40.  pis.  4-  1900. 

41.  GUIGNARD,  L.    La  double  fecondation  dans  le  mais.    Jour.  Bota- 

nique 15:  37-50.  1901. 

42.  -      — .    La  double  fecondation  dans  le  Naias  major.    Jour.  Bota- 

nique 15 :  205-213.  figs.  14.  1901. 

43.  .    Double  fecondation  chez  les  Renonculacees.    Jour.  Bota- 
nique 15:  394-408.  figs.  16.  1901. 

44.  HOLFERTY,  G.  M.     Ovule  and  Embryo  of  Potamogeton  natans. 

Bot.  Gazette  31 :  339-346.  pis.  2-3.  1901. 


186  MORPHOLOGY  OF  ANGIOSPERMS 

45.  LYON,   H.  L.    Observations    on    the    Embryogeny  of  Nelumbo. 

Minn.  Bot.  Studies  2 :  643-655.  pis.  48-50.  1901. 

46.  SMITH,  AMELIA  C.    The  Structure  and  Parasitism  of  Aphyllon 

uniflorum  Gray.  Contrib.  Bot.  Lab.  Univ.  Penn.  2:  111-121. 
pis.  13-15.  1901. 

47.  SCHNEGG,  H.    Beitrage    zur    Keniitniss    der    Gattung    Gunnera. 

Flora  90:  161-208.  figs.  28.  1902. 

48.  GUIGNARD,  L.     La  double  fecondation  chez  les  Solanees.    Jour. 

Botanique  16:  145-167.  figs.  45.  1902. 

49.  STRASBURGER,  E.     Ein  Beitrag  zur  Kenntniss  von  Ceratophyllum 

submersum  und  phylogenetische  Erorterungen.  Jahrb.  Wiss. 
Bot.  37:  477-526.  pis.  9-11.  1902. 

50.  HALL,  J.  G.    An  Embryological  Study  of  Limnocharis  emargi- 

nata.    Bot.  Gazette  33:  214-219.  pi.  9.  1902.  , 

51.  OVERTON,  J.  B.     Parthenogenesis  in   Thalictrum  purpurascens. 

Bot.  Gazette  33 :  363-375.  pis.  12-13.  1902. 

52.  COOK,  M.  T.    Development  of  the  Embryo-sac  and  Embryo  of 

Castalia  odorata  and  Nymphaea  advena.  Bull.  Torr.  Bot.  Club 
29:  211-220.  pis.  12-13.  1902. 

53.  JOHNSON,  D.  S.    The  Embryology  and  Germination  of  the  Genus 

Peperomia.     Abstract.  Science  15:  408-409.  1902. 

54.  IKEDA,  T.    Studies  in  the  Physiological  Functions  of  Antipodals 

and  related  Phenomena  of  Fertilization  in  Liliaceae.  1.  Tricyr- 
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3-6.  1902. 

55.  JOHNSON,  D.  S.     On  the  Development  of  Certain  Piperaceae.     Bot. 

Gazette  34:  321-340.  pis.  9-10.  1902. 

56.  FRYE,  T.  C.    A  Morphological  Study  of  Certain  Asclepiadaceae. 

Bot.  Gazette  34 :  389-413.  pis.  13-15.  1902. 

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58.  MURBECK,   S.     Ueber  die   Embryologie  von  Ruppia  rostellata 

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lished in  Bot.  Gazette  35 :  1903. 

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be  published  in  Bot.  Gazette  36:  1903. 


CHAPTEK    IX 


THE   EMBRYO 

IT  is  perhaps  impossible  at  present  to  formulate  any  defi- 
nite laws  for  the  development  of  the  embryo  of  Angiosperms. 
The  details  recorded  are  very  nu- 
merous  and  confusing,  the  great- 
est amount  of  variation  occurring 
in  allied  forms  and  even  in  the 
same  species.  Undue  attention 
probably  has  been  given  to  the 
succession  of  cell  divisions  in  the 
earliest  stages  of  the  embryo,  for  it 
is  at  this  very  period  that  the  em- 
bryo seems  to  be  peculiarly  respon- 
sive to  the  conditions  that  surround 
it.  What  the  conditions  are  that 
determine  that  a  cell-wall  in  a 
given  stage  of  the  embryo  shall 
run  now  in  one  plane,  now  in  an- 
other, or  even  shall  fail  to  develop, 
are  unknown ;  but  the  study  of  a 
large  series  of  embryos  makes  it 
evident  that  if  there  is  a  normal 
sequence  of  cell  divisions  it  is 
being  constantly  interfered  with. 

It     is     probable     that     when     these      FIG-   Bl.—  Cqpsella    Bursa  -  pastori*. 

minor  variations  are  neglected,  cer- 
tain laws  of  general  development 
will  appear  that  are  concerned  with 
the  organization  of  the  great  body  regions  rather  than  with  the 
succession  of  cell  divisions  (Fig.  81). 

187 


Photomicrograph  of  seed  showing 
embryo,  endosperm,  and  develop- 
ing testa ;  x  125. 


188  MORPHOLOGY  OF  ANGIOSPERMS 

.  In  general,  the  first  division  of  the  fertilized  egg  is  trans- 

verse, and  this  is  followed  by  one  or  more  divisions  in  parallel 
planes,  resulting  in  a  row  of  cells.  This  undifferentiated  group 
of  cells  is  conveniently  referred  to  as  the  proembryo.  In  gen- 
eral, the  proembryo  becomes  differentiated  into  suspensor  and 
embryo,  which  eventually  become  very  distinct,  although  their 
origin  is  variable.  This  means  that  in  general  all  the  product 
of  the  fertilized  egg  does  not  enter  into  the  structure  of  the 
embryo,  a  fact  also  true  of  most  Gymnosperms.  In  general, 
the  development  of  the  embryo  is  initiated  by  the  longitudinal 
division  of  the  end-cell  of  the  proembryo,  and  this  is  followed 
by  divisions  that  result  in  the  quadrant  and  then  the  octant 
stage.  It  is  in  the  octant  stage  that  periclinal  walls  may  cut  off 
the  dermatogen,  but  this  may  be  deferred  to  a  later  stage,  and 
is  often  irregular.  The  cells  of  the  dermatogen  divide  only  by 
anticlinal  walls,  but  the  inner  cells  continue  divisions  in  the 
three  dimensions,  and  soon  the  periblem  and  plerome  become 
distinguishable.  In  general,  the  end-cell  of  the  proembryo  does 
not  produce  all  of  the  embryo,  but  the  next  cell  divides  trans- 
versely, and  the  daughter-cell  adjacent  to  the  embryo  (hypo- 
physis) fills  out  the  periblem  and  dermatogen  of  the  root-tip. 
The  organization  of  the  growing  points  of  stem  and  cotyledon, 
in  relation  to  the  body  of  the  embryo,  are  so  radically  different 
in  Monocotyledons  and  Dicotyledons  that  no  general  statement 
concerning  it  is  possible. 

The  fact  remains  that  every  general  statement  given  above 
is  contradicted  by  well-known  and  bv.Jio  means  infrequent  ex- 
ceptions, and  even  the  distinction  beween^J&onocotyledons  and 
Dicotyledons  is  not  always  clear  in  the  embryo.  The  subject 
will  be  treated  in  some  detail  under  the  titles  Monocotyledons, 
Dicotyledons,  Parthenogenesis,  and  Polyembryony. 

MONOCOTYLEDONS 

The  embryo  of  Alisma  Plantago,  as  described  by  Hanstein  7 
and  Famintzin,17  has  long  been  taken  as  a  type  of  the  monocot- 
yledonous  embryo.  Among  recent  accounts  Schaffner's  43  de- 
scription of  the  embryo  of  Sagittaria  varidbilis,  following  his 
earlier  study  of  Alisma,™  is  the  most  complete,  and  while  it 
confirms  the  principal  features  of  the  earlier  accounts,  the  great 
improvement  in  technique  since  the  time  of  Hanstein  made  it 


TIG.  82. — Sagittaria  variabilis.  Development  of  embryo.  A,  proembryo  of  three  cells; 
a,  basal  cell  (in  all  figures) ;  J,  middle  cell  (dividing) ;  c,  terminal  cell  from  which 
the  cotyledon  is  derived;  #y,  synergid;  B,  same  stage,  but  terminal  cell  dividing; 
<?,  middle  cell  (b)  has  divided,"*  being  the  cell  from  whose  derivatives  the  stem-tip 
arises,  and  terminal  cell  (c)  dividing;  Z>,  both  cells  derived  from  b  are  dividing; 
£,  terminal  cell  has  given  rise  to  four  cells  (c),  and  the  region  derived  from  the 
middle  cell  (b)  has  developed  further ;  /",  showing  further  development  of  the 
middle  cell  region  (5),  while  the  terminal  cell  region  has  made  no  further  progress ; 
(r,  dermatogen  differentiated  in  the  terminal  cell  region  (c),  and  the  middle  region 
(b)  further  developed ;  H,  differentiation  of  dermatogen  beyond  the  terminal  region 
(c),  the  middle  region  (b)  showing  the  differentiation  between  hypocotyl  (A)  and 
region  producing  stem-tip ;  /,  more  advanced  stage,  showing  same  regions  as  in  H, 

and  the  plerome  and  periblem 
x  260. — After  SCHAFFKBR.*' 
189 


i^^ivu.   £/i  vsuuvi.u.g   oLcui-Li^/j    A^  iijui  c    aci>aiiv;c»J.    otiigc^  nui 

but  the  dermatogen  of  the  root-tip  not  yet  formed,  and 
undifterentiated.    A-F,  x  400 ;  G,  x  260 ;  H,  x  400 ;  /, 


190  MORPHOLOGY  OF  ANGIOSPERMS 

possible  to  correct  some  inaccuracies,  and  at  the  same  time  to 
show  that  the  early  divisions  of  the  fertilized  egg  do  not  follow 
such  a  definite  sequence  as  had  been  supposed.  The  following 
description  is  based  upon  his  account.  The  fertilized  egg  di- 
vides by  a  transverse  wall,  and  the  resulting  basal  cell  becomes 
large  and  vesicular,  but  does  not  divide.  The  apical  cell  divides 
by  a  transverse  wall  and  a  prpembryo  of  three  cells  is  the  result 
(Fig.  82).  The  terminal  cell  (Fig.  82,  c)  gives  rise  to  the  ter- 
minal cotyledon,  and  its  first  division,  which  may  take  place  im- 
mediately or  may  be  somewhat  delayed,  is  always  longitudinal. 
From  the  middle  cell  there  are  developed  the  lateral  stem-tip, 
the  root-tip,  the  hypocotyl,  and  all  of  the  suspensor  except  the 
vesicular  basal  cell.  The  middle  cell  divides  transversely,  and 
of  the  two  resulting  cells  the  one  next  the- terminal  cell  gives  rise 
to  the  stem-tip  (Fig.  82,  C',  s).  In  general,  the  ^differentiation 
is  basipetal,  proceeding  from  the  cotyledon  toward  the  suspen- 
sor. The  terminal  or  cotyledon  cell  having  divided  by  a  longi- 
tudinal wall,  the  next  division  is  transverse,  resulting  in  the 
quadrant  stage,  followed  by  the  octant  stage.  At  this  stage 
the  dermatogen  begins  to  be  differentiated,  appearing  first  in 
the  cotyledon  and  proceeding  toward  the  root  end  of  the  em- 
bryo. While  the  cell  from  which  the  stem-tip  arises  can  be 
identified  in  the  four-celled  proembryo,  it  is  only  in  much  later 
stages  (as  Fig.  82,  7)  that  it  is  readily  recognized.  In  the 
four-celled  proembryo  (Fig.  82,  (7)  the  cell  next  the  vesicular 
cell  divides  transversely ;  and  of  the  two  resulting  cells  the  one 
nearest  the  vesicular  cell  by  one  or  more  transverse  divisions 
gives  rise  to  a  filamentous  suspensor  of  two  to  six  cells;  from 
the  other  cell  are  developed  the  root  and  the  hypocotyl.  The 
dermatogen  is  usually  developed,  even  around  the  root-tip,  be- 
fore any  differentiation  of  periblem  and  plerome  can  be  dis- 
tinguished (Fig.  83). 

This  Alisma  type  has  proved  to  be  characteristic,  not  of 
Monocotyledons  in  general,  but  of  the  more  primitive  hydro- 
phytic  forms.  Its  main  features  are  an  undividing  and  usually 
much  enlarged  and  swollen  basal  cell  cut  off  by  the  first  division 
of  the  fertilized  egg,  and  a  proembryo  of  three  cells  whose  mid- 
dle cell  divides  basipetally  to  form  the  region  of  the  embryo 
behind  the  cotyledon,  and  also  forms  more  or  less  of  a  suspensor 
in  addition  to  the  large  basal  cell.  As  further  illustrations  of 


FIG.  83. — Sagittaria  variabllis.  Development  of  embryo.  A,  somewhat  advanced  stage 
showing  the  depression  in  which  the  stem-tip  develops;  x  216;  B,  about  the  same 
stage,  showing  the  entire  embryo ;  x  66 ;  £7,  later  stage,  with  dermatogen,  periblem, 
and  plerome  differentiated ;  x  216;  D,  the  lateral  stem-tip ;  x  140;  .£",  longitudinal 
section  of  a  ripe  seed  ;  x  26. — After  ScHAFFNER.43 

191 


192 


MORPHOLOGY  OF  ANGIOSPERMS 


it  we  would  cite  Sparganium  (Campbell55),  Potamogeton 
(Wiegand,63  Holferty71),  Z-annichellia  and  Naias  (Camp- 
bell 41),  Triglochin  (Hill  60),  and  Limnocharis  (Hall 82).  The 
last-mentioned  form  well  illustrates  that  the  general  type  may 
be  maintained,  and  at  the  same  time  there  may  be  no  regularity 
in  the  sequence  of  divisions  after  the  first  two.  In  fact,  the 
apical  cell  of  the  proembryo  of  Limnocharis  may  divide  by  a 
transverse,  oblique,  or  longitudinal  wall,  and  in  the  two  latter 
cases  the  cotyledon  and  stem-tip  are  both  terminal,  as  is  the 
case  also  in  Zannicliellia. 

Among  the  Gramineae  the  same  general  type  of  proembryo 
is  formed,  but  if  Avena  fatua  (Cannon65)  be  taken  as  repre- 
sentative of  the  general  situation,  the  origin  of  the  organs  of 
the  embryo  in  relation  to  the  cells  of  the  proembryo  is  quite 
different.  In  this  species  the  cotyledon  and  stem-tip  are  both 
derived  from  the  apical  cell,  the  entire  root-tip  (including  root- 
cap)  from  the  adjacent  cell,  and  the  coleorhiza  from  the  third 
cell,  the  suspensor  consisting  of  only  the  primary  basal  cell. 

Among  the  Araceae  a  very  different  type  of  embryo  is  indi- 
cated, but  so  few  forms  have  been  investigated  that  no  conclu- 
sion as  to  its  prevalence  in  the  family  is  safe.  In  1874  Hegel- 

maier  9  described  the  absence  of 
a  suspensor  in  Pistia,  the  fertil- 
ized egg  producing  a  spherical 
proembryo,  all  of  which  enters 
into  the  structure  of  the  embryo. 
Campbell  59  found  the  same  type 
of  embryo  in  Dieffenbachia,  Ag- 
laonema,  and  Lysichiton  (Fig. 
84),  and  states  that  in  the  seg- 
mentation of  the  egg  there  may 
be  two  transverse  divisions  be- 
fore any  vertical  division,  or  a 
regular  quadrant  may  be  formed 
as  in  the  ordinary  fern  embryo. 
Even  if  this  Pistia  type  should 
prove  to  be  characteristic  of  the 
Araceae,  it  is  not  restricted  to  them,  for  Humphrey38  has 
shown  that  the  embryos  of  the  Scitamineae  have  no  suspensors ; 
and  the  same  is  true  at  least  of  certain  orchids,  as  shown  by 


FIG.  84.  —  Lysichiton  kamtschatcense. 
Longitudinal  section  of  embryo  sur- 
rounded by  endosperm,  illustrating 
the  Pistia  type. — After  CAMPBELL." 


THE  EMBRYO 


193 


Treub 18   for  Listera  ovata   and  Epipactis  palustris,   and  by 
Leavitt 73  for  certain  species  of  Goodyera  and  Spirantlies.     It 
should  be  noted,  however,  that  in  Lemna   (Caldwell54),  the 
reduced    aquatic    ally 
of  the  Araceae,  a  mul- 
ticellular  suspensor  is 
formed,    the    embryo 
resembling    the    Lili- 
um type  described  be- 
low. 

Among  the  Lilia- 
ceae  a  third  type  of 
embryo  -  formation 
seems  to  prevail.  After 
the  first  segmentation 
of  the  fertilized  egg, 

which    is    transverse,  ^^^  /p. 

the    subsequent    divi-  ' 

sions  are  very  irregu- 
lar, being  transverse, 
oblique,  or  longitudi- 
nal in  either  cell,  re- 
sulting in  a  massive 
proembryo.  The  dif- 
ferentiation into  em- 
bryo and  suspensor  is 
late  and  irregular,  the 
suspensor  being  mass- 
ive, and  inclined  to 
continue  active  divi- 
sion until  the  end  of 
the  embryo-sac  is  oc- 
cupied by  a  spreading 
suspensor  tissue  (Fig.  85).  This  is  characteristic  of  Lilium 
(Coulter44),  Erythronium  (Schaffner 72),  Tulipa  (Ernst69}, 
and  probably  all  the  allied  forms,  and  the  meristematic  activity 
of  the  suspensor  is  apt  to  result  in  polyembryony  (see  below). 
Just  how  far  this  Lilium  type  of  embryo  is  represented  among 
Liliales  must  be  determined  by  future  investigation,  but  it  is 
distinct  enough  to  deserve  separate  mention. 


FIG.  85. — Lilium  philadelphicum.  A,  proembryo  of 
two  cells ;  x  300 ;  B,  middle  cell  of  filament  of 
three  cells  has  divided  longitudinally;  x  175;  (7, 
young  embryo  showing  massive  suspensor ;  x  300 : 
Z>,  older  embryo,  showing  different  form  of  sus- 
pensor ;  x  300. — After  COULTER.** 


194 


MORPHOLOGY  OF  ANGIOSPERMS 


FIG.   87.—  Gymnadenia  conopsea. 


Embryo  at  time  of 
shedding  seed.  After 
PFITZER  in  Engler 
and  Prantl's  Sat. 
Pflanzenfamilien. 


Among  the  Orchidaceae  there  is  the  greatest  amount  of 
variation  in  the  formation  of  the  embryo.  In  general  they  are 
characterized  by  very  poorly  developed  em- 
bryos, the  body  regions  not  being  differen- 
tiated, and  by  an  extraordinary  and  varied 
development  of  the  suspensor  as  an  hausto- 
rium.  As  already  mentioned,  however,  some 
of  them  (species  of  Lister  a*  Epipactis.  Good- 

P,    .         .,       xl  /-n.         FIG.  86.—  Listera  ovata. 

yera,  Spiranmes)   have  no  suspensor    (Fig. 

86).  Treub18  in 
1879  described  a 
number  of  forms  in 
which  the  filamen- 
tous suspensor  grows  out  of  the  micro- 
pyle,  often  branches,  and  embeds  it- 
self in  adjacent  nutritive  tissue,  such 
as  the  placenta.  He  found  that  in 
Phalaenopsis  grandiflora  branches  of 
the  suspensor  not  only  turn  toward 
the  micropyle,  but  also  toward  the 
embryo  and  finally  envelop  it.  Later 
the  same  investigator  24  described  the 
suspensor  of  Peristylis  grandis  as 
dividing  transversely,  growing  out 
through  the  micropyle,  and  embed- 
ding itself  by  pseudopodium-like  proc- 
esses in  the  placenta.  The  embryo 
of  Gymnadenia  conopsea,  as  described 
by  Marshall-Ward,20  is  probably  rep- 
resentative. The  first  division  of  the 
fertilized  egg  is  transverse,  the  basal 
cell  forming  a  chain-like  suspensor  of 
eight  to  ten  more  or  less  elongated 
cells  that  pushes  through  the  micro- 
pyle into  the  ovary  cavity,  and  the 
apical  cell  producing  a  perfect  octant 
stage,  the  dermatogen  being  cut  off 

jn  t^e  gixteen-celled   Stage    (Fig.    87). 

Leavitt  73  has  also  described  the  sus- 
—After  MARSHALL  WARD.™        pensors    of    Aplectrum    Jiiemale  ;    of 


THE  EMBRYO 


195 


Corattorhiza  mtdtiflora,  in  which  it  consists  of  two  very  long 
cells  and  embeds  its  tip  into  the  placenta;  of  Habenaria  tri- 
dentata,  and  of  H.  blephariglottis,  in  which  each  of  the  six  or 
seven  cells  of  the  suspensor  usually  sends  out  a  branch,  some  of 
them  short  and  reaching  the  integument,  others  elongated  and 
pas.- ing  parallel  with  the  suspensor  into  the  tissue  at  the  base 
of  the  funiculus. 

These  four  types  of  monocotyledonous  embryos,  which  for 
convenience  may  be  spoken  of  as  Alisma,  Pistia,  Lilium,  and 
Orcliid  types,  are,  of  course,  related  to  one  another  in  ways  that 
suggest  that  they  are  all  derivatives  of  one  general  monocotyled- 
onous form.  It  is  natural  to  assume  that  this  primitive  form 
is  more  nearly  represented  by  the  Alisma  type  than  by  any  of 


c  • 


FIG.  88. — Zannichellia  palustris.  Development  of  embryo.  A,  young  embryo ;  x  320; 
B,  later  stage,  showing  beginning  of  differentiation  into  stem-tip  («)  and  cotyledon  (c), 
both  coming  from  the  cells  derived  from  terminal  cell  of  proembryo ;  x  160 ;  C,  stem- 
tip  («)  and  cotyledon  (c)  clearly  differentiated ;  x  60. — After  CAMPBELL.41 

the  others,  not  merely  because  it  characterizes  the  primitive 
hydrophytic  forms,  but  also  because  it  is  the  simplest  type, 
and  the  others  may  well  be  modifications  of  it.  In  the  Pistia 
type  the  suspensor  is  suppressed ;  in  the  Lilium  type  it  becomes 
ma>>ive  and  meristematic ;  in  the  Orchid  type  it  is  developed 
as  a  special  haustorium  that  passes  out  of  the  ovule  on  account 
of  the  lack  of  endosperm,  and  perhaps  for  the  same  reason  the 
embryo  does  not  reach  the  stage  of  differentiating  organs. 

There  have  been  observed  certain  departures  from  the  mon- 
ocotyledonous type  of  embryo  that  deserve   special  mention. 


196  MORPHOLOGY  OF  ANGIOSPERMS 

In  1878  Solms-Laubach 15  stated  that  in  Dioscoreaceae  and 
certain  Commelinaceae  the  cotyledon  is  lateral  in  origin  rather 
than  terminal.  The  stem-tip  is  terminal  in  origin,  but  is  later 
forced  to  one  side  by  the  strong  growth  of  the  cotyledon  from 
beneath.  Such  a  departure  is,  of  course,  fundamental,  but  be- 
fore any  generalization  is  ventured  it  should  be  subjected  to  the 
most  critical  investigation.  Campbell  41  finds  that  in  Zanni- 
chellia  the  terminal  cell  of  the  proembryo  gives  rise  to  both  coty- 
ledon and  stem-tip,  the  separation  between  the  two  organs  being 
determined  by  the  first  vertical  division  of  the  terminal  cell 
(Fig.  88).  The  same  writer47  has  found  another  suggestive 
variation  in  Lilaea  subulata,  one  of  the  Juncaginaceae.  The 
embryonic  root-tip,  instead  of  being  directed  toward  the  sus- 
pensor,  is  directed  to  one  side,  almost  in  continuation  of  the 
axis  of  the  stem-tip.  This  lateral  origin  of  the  root  is  regarded 
by  Campbell  as  a  primitive  feature,  and  suggestive  to  him  of 
Isoetes.  In  other  particulars  the  embryo  is  of  the  Alisma  type. 
In  this  connection  the  recent  results  of  Murbeck  95  with  Ruppia 
are  suggestive.  He  confirms  the  account  of  Wille  that  a  pri- 
mary root  is  formed  at  the  base  of  the  embryo,  but  soon  dis- 
organizes, and  that  a  lateral  root,  formed  very  early,  is  the  first 
functional  one.  This  is  very  different  from  the  account  of 
Ascherson  in  Engler  and  PrantFs  "  Die  Natiirlichen  Pflanzen- 
familien,"  which  is  followed  in  Goebel's  "  Organography,"  ac- 
cording to  which  this  lateral  root  is  the  primary  root,  its  un- 
usual position  being  due  to  displacement. 

DICOTYLEDONS 

The  best-known  dicotyledonous  embryo  is  that  of  Capsella, 
as  described  by  Hanstein  7  and  Famintzin,17  and  it  has  been 
used  as  a  basis  of  comparison  ever  since.  To  illustrate  the 
earlier  stages  in  the  development  of  the  embryo,  therefore,  we 
have  made  a  rather  complete  series  of  camera  drawings  from 
sections  of  the  embryo  of  Capsella  (Figs.  89,  90 ;  see  also  Fig. 
81).  The  proembryo  is  a  filament  of  cells  of  varying  length. 
The  apical  cell  divides  first  longitudinally,  the  next  two  divi- 
sions being  longitudinal  and  transverse  in  either  order  and 
resulting  in  the  octant  stage.  Whether  the  transverse  division 
precedes  or  "follows  the  second  longitudinal  division,  it  sepa- 
rates the  cotyledonary  and  hypocotyledonary  regions  of  the  em- 


J 


FIG.  89. — Capsella  Bursa-pastoris.  A,  first  division  of  terminal  (embryo)  cell;  B,  quad- 
rant stage ;  (7,  octant  stage ;  Z>,  differentiation  of  dermatogen ;  E,  differentiation 
of  periblem  and  plerome  (latter  shaded) ;  F,  completion  of  periblem  of  root ;  G-y 
beginning  of  differentiation  of  dermatogen  of  root-tip  (indicated  by  mitotic  figure) ; 
H,  later  stage,  showing  plerome,  periblem,  dermatogen,  and  one  layer  of  root-cap 
(plerome  and  dermatogen  shaded);  7,  two  layers  in  root-cap  (the  plerome  and 
portion  of  dermatogen  derived  from  hypophysis  shaded) ;  J,  young  embryo  sur- 
rounded by  endosperm ;  walls  of  ovary  also  shown  ;  x  400. 

197 


198 


MORPHOLOGY  OF  ANGIOSPERMS 


bryo.  In  the  octant  stage  the  dermatogen  begins  to  be  differ- 
entiated, the  periclinal  divisions  appearing  first  in  the  terminal 
octants  and  proceeding  toward  the  root  end  of  the  embryo.  The 
differentiation,  however,  is  almost  simultaneous,  so  that  the 
dermatogen  is  soon  completed  except  that  of  the  root-tip,  which 
is  derived  from  the  adjacent  cell  of  the  suspensor,  and  appears 
comparatively  late.  The  periblem  and  plerome  are  differen- 
tiated early  from  the  tissue  within  the  dermatogen.  The  stem- 
tip  and  cotyledons  are  derived  from  the  four  apical  octants,  and 
the  bulk  of  the  hypocotyl  from  the  four  basal  octants.  The 
root-tip,  however,  is  completed  by  the  adjacent  cell  of  the  sus- 


FIG.  90. — Capsella  Bursa-pastoris.  Series  showing  contribution  of  upper  cell  of  suspen- 
sor to  embryo  (plerome  and  dermatogen  shaded):  s,  upper  cell  of  suspensor;  7/, 
hypophysis;  d,  dermatogen ;  d',  portion  of  dermatogen  derived  from  hypophysis; 
pi,  plerome ;  p,  periblem ;  p\  portion  of  periblem  derived  from  hypophysis  ;  x  400. 

pensor  (Fig.  90,  s).  This  cell  divides  transversely,  the  basal 
daughter-cell  taking  no  part  in  the  formation  of  the  embryo, 
but  the  other  daughter-cell  (hypophysis  of  Hanstein)  filling 
out  the  periblem  and  dermatogen  of  the  root-tip.  The  hypophy- 
sis divides  transversely,  the  daughter-cell  next  the  embryo  com- 
pleting the  periblem  of  the  root.  The  other  daughter-cell  by 
two  longitudinal  divisions  gives  rise  to  a  plate  of  four  cells, 
each  of  which  divides  transversely,  the  plate  of  four  cells  toward 
the  embryo  completing  the  dermatogen  of  the  root-tip,  and  the 
other  plate  constituting  the  first  layer  of  the  root-cap. 


THE  EMBRYO 


199 


Tin-  type  of  embryo,  called  for  convenience  the  Capsella 
type,  is  well  represented  throughout  the  Dicotyledons,  and,  so 
far  as  we  have  the  means  to  judge, 
seems  to  be  the  prevalent  type,  subject, 
of  course,  to  variation  in  detail.  For 
example,  it  occurs  in  Salix  (Chamber- 
lain42),  in  which  it  is  questionable 
whether  the  hypophysis  contributes  to 
the  periblem;  in  Ranunculus  (Coul- 
ter 4*)  and  Thalictrum  (Overton83), 
in  the  latter  case  the  suspensor  some- 
times becoming  a  massive  and  twisted 
organ;  in  Alyssum  (Riddle51),  which 
almost  exactly  repeats  the  embryogeny 
of  Capsella;  in  Sium,  in  which  there 
is  a  very  long  suspensor;  in  Sarcodes 
(Oliver30);  in  Aricennia  (Treub24); 
in  Trapella  (Oliver29),  in  which  there 
is  a  remarkably  long  suspensor  with  an 
enormously  elongated  basal  cell ;  and  in 
Senecio  (Mottier*4),  Silphium  (Mer- 
rell61),  and  Taraxacum  (Schwere  40). 
Among  the  Rosaceae  Pechoutre  87  has 
recorded  a  wide  variation  in  the  struc- 
ture of  the  suspensor,  different  genera 
showing-  every  gradation  between  a  sim- 
ple filamentous  suspensor  (Fragariay 
Geum)  and  one  that  is  short  and  mass- 
ive (  Crataegus,  Amygdalus).  These 
examples  represent  all  regions  of  Dicot- 
yledons ;  and  while  there  are  differ- 
ences as  to  the  division  of  the  basal 
suspensor-cell,  the  length  of  the  sus- 
pensor, and  the  succession  of  walls  in 
the  apical  cell  (embryo-cell)  of  the  pro- 

•1,1  -i*  i         FIG.    91.  —  Loranthus   sphaero- 

embryo,  the  general  type  remains  the  carpus  ^  young  e^bryo; 
same,  and  resembles  most  nearly  the  x  190 ;  B,  later  stage,  show- 
AUxwa  type  among  Monocotvledons.  in=  extreme  lengthening  of 

T          i  i  •    •  At  •  '•!•  the   two  bulbous   suspensor- 

In  addition  to  this  prevailing  type,      cells;  ^  embryo;  ^  suspenfc 
there  are  modifications  of  it  that  su°:-      sor;  x  120.— 

^ 

14 


200 


MORPHOLOGY  OF  ANGIOSPERMS 


gest  as  wide  a  range  of  variation  as  among  Monocotyledons, 
though  not  so  clearly  related  to  great  groups. 

In  Geranium,  as  has  long  been  known,  while  the  Capsella 
type  is  maintained  in  general,  there  is  no  hypophysis,  the  root- 
tip  being  covered  by  the  tissue  of  a  massive  suspensor. 

In  Peperomia  pellucida  Campbell  56  and  Johnson  62  have 
both  observed  that  the  first  segmentation  of  the  fertilized  egg 
is  vertical,  followed  by  a  transverse  division,  and  that  there  is 
no  indication  of  a  suspensor. 

In  Loranthus  sphaerocarpus  Treub  22  has  described  the  first 
division  of  the  fertilized  egg  as  vertical,  as  in  Peperomia,  but 
followed  by  transverse  divisions,  so  that  the  proembryo  resem- 
bles two  filaments  lying  side  by  side  (Fig.  91).  The  two  basal 
cells  elongate  enormously,  forming  a  suspensor  as  in  Gymno- 
sperms,  whose  length  is  increased  by  the  moderate  elongation 
of  the  second  pair  of  cells,  and  which  becomes  more  or  less  tor- 
tuous, the  cells  twisting  about  one  another.  In  L.  pentandrus 
(Treub26)  the  elongating  suspensor  early  forces  the  embryo 
against  the  resistant  base  of  the  sac,  where  it  becomes  much 
flattened  out,  and  for  a  time  bears  little  resemblance  to  an  em- 


—  s 


--  e 


FIG.  92. — Loranthus  pentandrus.  A,  young  embryo  advancing  into  endosperm;  thick- 
walled  tissue  at  base  of  sac  deeply  shaded ;  e,  embryo ;  #,  suspensor ;  x  88 ;  B,  later 
stage,  the  embryo  has  reached  the  resistant  base  of  the  sac  and  has  become  flattened 
out ;  x  144.— After  TBEUB .«« 

bryo  (Fig.  92).  In  Myoporum,  as  described  by  Billings,70  the 
suspensor  is  also  extremely  long  and  filamentous,  forcing  the 
young  embryo  down  into  the  principal  mass  of  endosperm, 


THE  EMBRYO 


201 


which  is  at  a  considerable  distance  from  the  micropylar  end 

of  the  embryo-sac  (Fig.  93). 

In  Xelumbo  Lyon  75  states  that  there  is  no  suspensor,  but 

that  the  divisions  of  the  egg  result  in  a  large  spherical  body 

that  is  still  undifferentiated  when 
consisting  of  several  hundred  cells, 
recalling  the  Pistia  type  among 
Monocotyledons.  In  Ceratophyl- 
lum  demersum  Strasburger  84  has 
found  the  same  undifferentiated 


FIG.  93. — Myoporum  serratum.  Young 
embryo  with  very  long  suspensor 
embedded  in  endosperm.  —  After 
BILLINGS.™ 


B 

•  FIG.  94. — Barringtonia  Vriesei.  A,  young 
proembryo;  B,  later  stage,  showing 
differentiation  into  embryo  (e)  and 
suspensor  (s) ;  x  104. — 


spherical  embryo  of  hundreds  of  cells  and  with  no  suspen- 
sor ;  while  in  NympJiaea  Conard  81  finds  the  same  type,  but 
associated  with  it  is  a  suspensor  consisting  of  a  row  of 
three  to  five  cells.  In  HecJceria  (Piperaceae)  Johnson  86  has 
described  the  early  stage  of  the  embryo  as  a  globular  mass 
composed  of  several  hundred  cells  undifferentiated  except  for 
a  rudimentary  suspensor;  and  in  Cynomoriwn  (Balanophora- 
ceae)  Juel 93  describes  the  embryo  as  a  small  spherical  mass 
of  cells  with  no  suspensor  and  no  differentiation  into  body 
regions. 

In  Barringtonia  Vriesei,  one  of  the  Myrtaceae,  Treub 27 
has  described  a  broad  mass  of  tissue  almost  filling  the  micropy- 
lar end  of  the  embryo-sac.  At  first  the  mass  is  homogeneous, 


202 


MORPHOLOGY  OF  ANGIOSPERMS 


B 


and  it  is  only  late  that  the  embryo  becomes  differentiated  from 
the  massive  suspensor  (Fig.  94). 

In  the  Kubiaceae  Lloyd  57-  85  has  described  a  remarkable  de- 
velopment of  the  suspensor,  which  in  many  members  of  the  group 

acts  as  a  haustori- 
um  (Fig.  95).  In 
Vaillantia  hispida 
the  large  suspensor 
cells  near  the  em- 
bryo are  clustered 
like  "  a  bunch  of 
grapes/'  while  far- 
ther down  a  single 
elongated  cell  forms 
a  point  of  attach- 
ment. In  Asperula 
the  scanty  cyto- 
plasm and  the  nu- 
cleus are  found  at 
the  distal  ends  of 
the  haustorial  cells 

FIG.  95.— .4,  Vaillantia  hispida.    Young  embryo  showing  of      the      SUSpenSOr, 

haustorial  suspensor ;  x  375 ;  after  LLOYD.CT    J9,  Aspe-  recalling     a     COndi- 

rula  azurea     Young  embryo  with  haustoria  from  sus-  ^  ^^  ^  ^^ 
pensor  highly  developed ;  alter  LLOYD.35 

described    for    root 

hairs.  It  is  worthy  of  note  that  among  the  Spermacoceae  and 
in  Houstonia  there  is  a  complete  absence  of  these  striking 
adaptive  characters  of  the  suspensor. 

It  is  among  the  Leguminosae,  however,  that  the  greatest 
amount  of  variation  in  embryogeny  exists  and  the  most  unusual 
forms  appear,  as  shown  by  Guignard  21  (Figs.  96-98).  It  is 
impossible  to  give  in  a  brief  account  any  adequate  idea  of  the 
amount  of  variation  displayed  by  the  nearly  forty  species  Guig- 
nard has  described,  involving  in  the  main  the  character  of  the 
proembryo  and  the  final  condition  of  the  suspensor.  In  1880 
Strasburger  19  had  called  attention  to  the  fact  that  the  cells  of 
the  very  long  suspensor  of  Lupinus  separate  early,  leaving  the 
embryo  free  and  some  distance  from  the  micropylar  extremity 
of  the  sac.  This,  however,  is  but  one  phase  of  the  embryogeny 
of  the  Leguminosae.  In  every  case  the  first  segmentation  of  the 


THE  EMBRYO 


203 


egg  is  transverse,  but  this  may  be  followed  either  by  longi- 
tudinal or  transverse  divisions,  in  the  former  case  generally  re- 
sulting in  a  massive  and  often  globular  proembryo,  in  the  latter 
resulting  in  an  extraordinarily  long  and  conspicuous  filamen- 
tous proembryo.  In  almost  every  case  the  suspensor-cells  are 
more  or  less  swollen  and  bladdery  and  surcharged  with  nutritive 
material,  forming  a  conspicuous  nutritive  tissue  for  the  embryo. 
The  two  types  of  proembryo  may  be  illustrated  as  follows : 

As  illustrations  of  the  massive  proembryo,  in  which  the  sus- 
pensor  and  embryo  are  gradually  differentiated,  but  are  never 
very  distinct  externally  except  by  a  constriction  between  them, 
may  be  cited  species  of  Acacia  and  Mimosa]  Cercis  siliquas- 
trum,  in  which  the  oblong  proembryonic  mass  broadens  at  each 
end  to  form  the  embryo  and  suspensor ;  Caesalpinia  mimosoides, 
in  which  the  embryo  becomes  distinct  rather  early  as  the  region 
of  more  actively  dividing  cells;  Cytisus  Laburnum,  in  which 
the  suspensor  becomes  a  great  mass  of  loose  rounded  cells  re- 
sembling a  globular  cluster  of  berries;  Anthyllis  tetrapliylla, 
in  which  the  suspensor  is  like  that  of  Cytisus,  but  the  clustered 


FIG.  96.  —  Embryos  of  Leguminosae.  A,  Cercis  siliquastrum,  with  suspensor  and  embryo 
developing  about  equally  ;  x  270  ;  B-E,  Spartlum  junceum  :  e,  embryo  ;  «,  suspen- 
sor ;  x  300.  —  After 


cells  are  much  fewer  in  number  ;  Spartium  junceum  and  Trifo- 
lium  resupinatum,  in  which  the  massive  proembryo  seems  to 
constrict  as  in  Cercis,  but  the  suspensor  as  the  cotyledon  stage 
approaches  is  smaller  than  the  embryo;  Tetragonolobus  pur- 
pur  ens,  in  which  the  larger  part  of  the  massive  proembryo  be- 
comes the  suspensor;  Hedysarum  coronarium  and  Arachis  hypo- 


204 


MORPHOLOGY  OF  ANGIOSPERMS 


gaea ;  Onobrychis  petraea,  in  which  the  proembryo  is  a  globular 
mass  of  cells;  and  Phaseolus  multiflorus  and  Erythrina  crista- 

galli,  in  which  the  massive  pro- 
embryo  is  elongated  and  there 
is  no  superficial  separation  be- 
tween embryo  and  suspensor. 

In  case  two  or  more  of  the 
first  divisions  are  transverse, 
forming  a  filamentous  proem- 
bryo, the  end-cell  forms  the  en- 
tire embryo,  the  suspensor-cells 
becoming  relatively  extremely 
large  and  bladdery  inflated. 
Two  general  types  may  be  noted. 
In  Orobus  angustifolius,  0.  au- 
reus,  Pisum  sativum,  Lathyrus 
heterophyUus,  L.  odoratus,  Er- 
vum  Ervilia,  and  View  narbon- 
nensis,  a  proembrvo  consisting 
of  a  row  of  three  cells  divides 
longitudinally;  the  two  basal 
cells  become  much  elongated, 
bladdery  inflated,  and  multinu- 
cleate;  the  middle  pair  become 
bladdery  inflated  and  multinu- 
cleate ;  and  at  the  end  of  such  a 
suspensor  the  terminal  pair  of 
cells  organize  a  small  round, 

oval,  or  elongated  embryo.  In  Cicer  arietinum  it  is  interesting 
to  note  that  the  same  huge  suspensor  and  small  embryo  appear, 
but  the  suspensor-cells  instead  of  becoming  multinucleate 
divide,  forming  a  many-celled  massive  suspensor.  In  the  other 
type,  transverse  divisions  continue  until  the  proembrvo  consists 
of  a  long  filament  of  cells,  all  of  which,  excepting  the  end-cell, 
form  a  suspensor,  as  in  Medicago  falcata-,  Galega  orientalis,  in 
which  the  long  suspensor  finally  becomes  massive  by  longitu- 
dinal divisions;  and  Ononis  fruticosa,  in  which  the  suspensor- 
cells  become  very  large  and  rounded,  forming  a  chain  that 
finally  breaks  up.  In  Ononis  alopecuroides,  however,  the  sus- 
pensor is  reduced  to  a  single  cell.  The  genus  Lupinus  is  espe- 


FIG.  97. — Embryos  of  Leguminosae.  A, 
Orobus  angustifolius,  with  suspensor 
of  three  multinucleate  cells;  x  336. 
j5,  Cicer  arietinum,  with  large  multi- 
cellular  suspensor  and  small  embryo 
(e) ;  x  160. — After  GuiGNARD.31 


THE  EMBRYO 


205 


cially  characterized  by  its  extensive,  worm-like,  and  large-celled 
suspensors,  whose  cells  often  break  apart.  The  suspensor  may 
consist  of  twenty  pairs  of  elongated  cells,  forming  a  tortuous 
filament  extending  the  entire  length  of  the  embryo-sac,  with  a 
very  small  embryo  at  the  tip,  as  in  L.  subcarnosus ;  or  it  may  be 
a  filament  of  short,  very  broad  cells,  suggesting  a  leech  in  ap- 
pearance, as  in  L.  pilosus;  or  it  may  be  a  loose,  large-celled 
tissue  lying  along  the  cavity  of  the  embryo-sac,  actively  dividing 
and  more  or  less  surrounding  the  late-forming  embryo  with  its 
rounded  cells,  that  finally  break  apart  and  become  disorganized, 
as  in  L.  polyphyUus,  L.  mutabilis,  L.  truncatus,  etc. 

The  degree  of  development  of  the  embryo  is  extremely  vari- 
able.   In  some  cases  a  plumule  with  several  leaves  is  formed,  and 


FIG.  93. — Embryos  of  Leguminosae.  A,  Lupinus  subcarnosus,  with  long  sinuous  sus- 
pensor and  small  four-celled  embryo  (e) ;  x  270.  £,  L.  luteus,  with  many  suspensor- 
cells  binucleate ;  x  160.  C,  L.  pilosus,  with  some  basal  suspensor-cells  isolated ; 
x  80.— After  GUIGNARD." 

even  lateral  roots  appear,  as  in  Gramineae,  Impatiens,  Cucu.r- 
bita,  Trapa,  etc.;  while  in  many  parasites  and  saprophytes  the 
embryo  is  represented  only  by  an  undifferentiated  mass  of  cells. 


206  MORPHOLOGY   OF  ANGIOSPERMS 

Among  ,the  Monocotyledons  such  undifferentiated  embryos  ap- 
pear among  Orchidaceae  and  Burmanniaceae,  in  the  former 
family  the  primary  root  never  appearing;  but  they  are  even 
more  numerous  among  Dicotyledons.  Goebel  28  states  that  the 
embryo  of  Monotropa  consists  of  five  to  nine  cells,  and  that  of 
Pyrola  secunda,  quoting  from  Hofmeister,  of  eight  to  sixteen 
cells.  The  entirely  undifferentiated  embryo  of  Aphyllon  uni- 
florum  has  been  noted  by  Miss  Smith  78 ;  and  the  embryos  of 
Orobanchaceae  (Koch14),  and  of  Balanophoraceae  and  Cytiria- 
ceae  (Solms-Laubach  8),  consist  of  a  very  small  mass  of  tissue. 
In  this  connection  it  should  be  noted,  however,  that  in  Cuscuta- 
and  Viscum  the  embryos  are  large  and  well  developed.  In 
some  non-parasitic  forms  also  poorly  developed  embryos  occur, 
as  in  Utricularia  (Kamienski J1),  in  which  the  embryo  develops 
no  root-tip  but  produces  a  large  number  of  peculiar  leaves. 

The  appearance  of  a  single  cotyledon  in  the  embryos  of 
certain  Dicotyledons  has  naturally  attracted  attention.  As  a 
prefatory  illustration,  it  may  be  observed  that  in  Trapa  natrtns, 
one  cotyledon  is  much  smaller  than  the  other,  and  this  suggests 
the  possibility  of  further  abortion  and  even  of  suppression  of 
one  of  the  cotyledons.  In  Ranunculus  Ficaria  Irmisch  l  long 
ago  reported  the  occurrence  of  a  single  cotyledon  sheathing 
below,  and  Erianthis  hiemalis,  Corydalis  cava,  and  Carum 
(Bunium)  bulbocastanum  have  also  been  included  in  the  list 
of  "  pseudo-monocotyledons."  In  the  case  of  C.  'bulbocastanum 
Hegelmaier  10  discovered  that  the  apparently  single  and  ter- 
minal cotyledon  is  accompanied  by  a  second  almost  completely 
aborted  and  lateral  cotyledon.  All  of  these  forms  have  been 
investigated  recently  by  Schrnid,91  who  discovered  that  in  Eri- 
anlhis  hiemalis  the  two  cotyledons  are  of  unequal  size ;  that  in 
Ranunculus  Ficaria  there  is  hardly  a  trace  of  a  second  cotyle- 
don, and  that  this  trace  was  probably  mistaken  by  Irmisch  1 
for  a  sheathing  base ;  and  that  in  Corydalis  cava  there  is  only  a 
slight  protuberance  to  represent  the  second  cotyledon,  the  func- 
tioning one  in  its  growth  gradually  assuming  a  more  terminal 
position  and  thrusting  the  stem-tip  to  an  apparently  lateral  posi- 
tion, but  in  C.  nobilis  and  C.  lutea  the  normal  development  of 
cotyledons  is  found.  In  Cyclamen  persicum,  also,  Schmid 
found  embryos  in  ripe  seeds  with  no  trace  of  a  second  cotyle- 
don. From  these  cases  it  is  evident  that  in  certain  dicotvled- 


THE  EMBRYO  207 

onous  forms  there  may  be  early  abortion,  which  may  even 
approach  suppression,  of  one  of  the  cotyledons ;  and  that  ^n 
consequence  of  this  the  single  functional  cotyledon  may  appear 
terminal  and  the  stem-tip  lateral.  To  call  such  cases  "  pseudo- 
monocotyledons/'  however,  is  not  consistent  with  the  real  nature 
of  the  monocotyledonous  embryo.  It  is  of  interest  to  note,  how- 
ever, that  Miss  Sargant,94  in  her  recent  study  of  the  "'  mono- 
cotyledonous Dicotyledons,"  a  special  case  being  made  of  Ranun- 
culus Ficaria,  has  concluded  that  the  apparently  single  cotyle- 
don is  a  fusion  of  two. 

The  peculiar  development  of  the  cotyledons  of  Nelumbo  has 
suggested  to  Lyon  74'  75  that  they  represent  a  single  two-lobed 
cotyledon,  and  that  this  fact,  along  with  certain  anatomical 
details,  should  place  Nelumbo  among  the  Monocotyledons.  In 
its  early  stage  he  represents  the  proembryo  as  being  a  many- 
celled  spherical  body,  that  later  becomes  a  flattened  mass  filling 
the  micropylar  extremity  of  the  sac.  The  stem-tip  arises  from 
the  free  surface  toward  one  side,  and  a  cotyledonary  ridge 
arises  behind  it  as  a  crescentic  mound  of  tissue,  whose  wings 
finally  extending  around  form  a  sheath  about  the  stem-tip. 
By  the  development  of  two  growing  points  on  this  cotyled- 
onary sheath  two  lobes  appear  and  develop  rapidly,  the  two 
becoming  concave  and  surrounding  the  plumule  as  a  tube.  The 
evidence  in  favor  of  a  single  cotyledon  seems  convincing  until 
this  embryogeiiy  is  compared  with  that  of  Nymphaea,  as  has 
been  done  by  Conard.81  In  this  genus  the  same  spherical  mul- 
ticellular  proembryo  appears,  two  opposite  and  symmetrical 
cotyledons  with  the  stem-tip  between  them  arising  from  the  free 
side,  and  the  basal  portion  forming  the  hypocotyl.  At  maturity 
the  cotyledons  become  concave  and  inclose  the  plumule,  just 
as  in  Nelumbo.  There  can  be  no  question  that  the  two  genera 
are  closely  related ;  and  since  the  embryogeny  of  Xympliaea  is 
typically  dicotyledonous,  it  follows  that  that  of  Nelumbo  must 
be  only  a  modification  of  it,  and  that  for  some  reason  the  stem- 
tip  does  not  occupy  its  usual  central  position,  and  the  two 
cotyledons  arise  for  a  time  en  masse,  as  in  the  case  of  petals 
in  sympetaly.  Conard  calls  attention  to  such  behavior  on  the 
part  of  the  cotyledons  of  Tropaeolum,  which  appear  "  connate- 
perfoliate  "  about  the  hypocotyl ;  and  also  to  the  fact  that  Hegel- 
maier  noted  the  complete  fusion  of  the  cotyledons  along  one 


208  MORPHOLOGY  OF  ANGIOSPERMS 

edge  in  Nuphar  lutea.  In  his  recent  study  of  Ceratophyllum 
Strasburger  84  finds  that  the  embryo  in  its  earlier  stages  bears 
a  striking  resemblance  to  that  of  Nelumbo,  there  being  a  large 
spherical  mass  of  cells  with  no  suspensor  (Fig.  80).  The  em- 
bryo of  Nelumbo  has  the  rudiment  of  a  root,  although  it  never 
develops,  the  first  functional  roots  coming  from  the  stem  above 
the  cotyledon  (Fig.  80,  s).  In  Ceratophyllum  the  reduction 
due  to  the  water  habit  has  gone  further,  not  even  the  rudiment 
of  a  root  appearing  in  the  embryo.  The  two  cotyledons  of 
Ceratophyllum  so  strongly  resemble  the  condition  in  Neluinbo, 
that  Strasburger,  after  examining  the  embryo  of  the  latter,  was 
forced  to  believe  that  here  also,  as  in  Ceraiophyllum,  there  are 
two  cotyledons. 

The  occasional  occurrence  of  a  whorl  of  three  cotyledons 
has  been  reported  for  Quercus,  Amygdalus,  Phaseolus,  etc.,  and 
many  other  cases  are  given  by  Braun.6 

In  this  connection,  recent  suggestions  as  to  the  phylogeny 
of  the  cotyledon  may  be  referred  to.  The  current  opinion  re- 
gards it  as  a  modified  foliage  leaf,  and  this  is  borne  out  in  the 
majority  of  Dicotyledons  by  the  assumption  of  the  foliage  func- 
tion. The  terminal  cotyledon  of  Monocotyledons,  however, 
seems  to  belong  to  a  different  category,  and  to  hold  no  relation 
to  a  foliage  leaf  or  to  a  foliar  member  of  any  description.  In 
a  recent  paper  H.  L.  Lyon  88  develops  the  idea  that  the  cotyle- 
don of  Angiosperms  is  phylogenetically  related  to  the  sucking 
organ  known  as  the  "  foot  "  among  Bryophytes  and  Pterido- 
phytes.  His  own  summary  makes  his  position  clear: 

(1)  The  typical  embryos  of  the  Pteridophytes  and  Angiosperms 
differentiate  into  three  primary  members,  the  cotyledon,  stem,  and 
root ;  (2)  cotyledons  are  not  arrested  leaves,  but  are  primarily  hausto- 
rial  organs  originating  phylogenetically  as  the  nursing-foot  in  the 
Bryophytes  and  persisting  throughout  the  higher  plants  ;  (3)  the  mono- 
cotyledonous  condition  is  the  primitive  one  and  prevails  in  the  Bryo- 
phytes, Pteridophytes,  Monocotyledons,  and  some  Gymnpsperms ;  the 
two  (sometimes  more)  cotyledons  of  the  Dicotyledons  are  jointly  the 
homologue  of  the  single  cotyledon  of  the  Monocotyledons ;  (4)  the 
cotyledon  always  occurs  at  the  base  of  the  primary  stem  ;  (5)  the  hypo- 
cotyl  is  a  structure  peculiar  to  the  Angiosperms,  being  differentiated 
between  the  primary  stem  and  root ;  (6)  the  so-called  cotyledon  of 
the  Pteridophytes  arid  Gymnosperms,  with  the  probable  exception  of 
Ginkgo  and  the  Cycads,  are  true  foliage  leaves. 


THE  EMBRYO  209 

The  same  general  idea  has  been  expressed  by  Balfour,80  as 
the  following  quotations  show: 

"  We  ought,  I  think,  to  look  upon  the  embryo  as  a  protocorm  of 
embryonic  tissue  adapted  to  a  seed-life.  Under  the  influence  of  its 
heterotrophic  nutrition  and  seed-environment  it  may  develop  organs 
not  represented  in  the  adult  plant  as  we  see  in,  for  instance,  the  embry- 
onal intraovular  and  extraovular  haustoria  it  often  possesses.  There 
is  no  reason  to  assume  that  there  must  be  homologies  between  the 
protocorm  and  the  adult  outside  an  axial  part  with  its  polarity.  There 
may  be  homologous  organs  ;  but  neither  in  ontogeny  nor  in  phylogeny 
is  there  sufficient  evidence  to  show  that  the  parts  of  the  embryo  are  a 
reduction  of  those  of  the  adult." 

"That  the  cotyledons,  primarily  suctorial  organs,  should  change 
their  function  and  become  leaf-like  under  the  new  conditions  after 
germination  is  no  more  peculiar  than  that  the  hypocotyl  should  take 
the  form  of  an  epicotylar  internode,  from  which  it  is  intrinsically 
different  as  the  frequent  development  upon  it  of  hypocotylar  buds 
throughout  its  extent  shows." 

"  The  protocorm  has,  I  believe,  developed  along  different  lines  in 
the  Dicotyledons  and  Monocotyledons.  This  has  been  to  the  advan- 
tage of  the  former  in  the  provision  that  has  been  made  for  rapid  as 
opposed  to  sluggish  further  development.  Confining  ourselves  to  the 
general  case,  the  axial  portion  of  the  protocorm  of  the  Dicotyledon, 
the  hypocotyl,  bears  a  pair  of  lateral  outgrowths,  the  cotyledons,  and 
terminates  in  the  plumular  bud  and  in  the  primary  root  respectively. 
The  cotyledons  are  its  suctorial  organs,  and  the  hypocotyl  does  the 
work  of  rupturing  the  seed  and  placing  the  plumular  bud  and  root  by 
a  rapid  elongation  which  commonly  brings  the  plumular  bud  above 
ground,  protected,  it  may  be,  by  the  cotyledons.  These  latter  may 
then  become  the  first  assimilating  organs  unlike  or  like  to  the  epico- 
tylar leaves.  In  the  Monocotyledons  the  axial  portion  of  the  proto- 
corm has  usually  no  suctorial  outgrowths.  Its  apex  and  usually  its 
base  also  are  of  limited  growth.  The  plumular  bud  is  a  lateral  devel- 
opment, and  the  primary  root  often  an  internal  one.  The  suctorial 
function  is  performed  by  the  apex  of  the  protocorm,  termed  here  also 
the  cotyledon." 

"I  use  the  term  purely  as  an  objective  designation,  and  in  the 
original  meaning  of  the  suctorial  organ  in  the  embryo.  This  terminal 
cotyledon  in  the  Monocotyledons  is  not  a  leaf  nor  the  homologue  of 
the  lateral  cotyledons  in  the  Dicotyledons." 

An  explanation  of  the  terminal  cotyledon  of  Monocotyledons 
has  been  suggested  by  Miss.  Sargant  89  in  her  study  of  the  seed- 
lings of  Liliaceae.  In  AnemarrJiena  she  finds  the  cotyledon 


210  MORPHOLOGY   OF  ANGIOSPERMS 

traversed  by  two  opposed  vascular  bundles,  which  suggest  the 
fusion  of  two  organs  and  a  derivation  from  the  dicotyledonous 
condition.  This  position  is  further  strengthened  by  the  well- 
known  tendency  among  certain  Dicotyledons  for  the  cotyledons 
to  become  more  or  less  completely  fused  (see  Chapter  XV). 

The  whole  problem,  however,  is  too  indefinite  as  yet,  and 
the  data  are  too  few  to  permit  well-grounded  conclusions,  but  it 
is  well  worth  consideration. 

PARTHENOGENESIS 

The  term  parthenogenesis  was  once  very  loosely  applied, 
including  all  cases  of  the  appearance  of  embryos  without  fer- 
tilization. Strictly,  however,  it  includes  only  those  cases  in 
which  the  normal  egg  produces  an  embryo  without  fertilization, 
and  this  phenomenon  has  thus  far  been  demonstrated  in  only 
three  angiospermous  genera,  to  be  described  below.  Apogamy, 
being  the  production  of  a  sporophyte  by  a  gametophyte  without 
the  act  of  fertilization,  of  course  includes  parthenogenesis,  but 
the  production  of  sporophytes  by  gametophytic  structures 
other  than  the  egg  may  for  convenience  be  distinguished  as 
vegetative  apogamy.  In  this  category  would  be  included  all 
cases  of  embryos  derived  from  unfertilized  synergids,  antip- 
odals,  and  endosperm,  the  last-named  structure  being  included 
or  not  dependent  upon  one's  view  as  to  its  morphological  char- 
acter. When  an  unfertilized  synergid  produces  an  embryo,  it 
might  be  claimed  that  it  is  not  a  case  of  vegetative  apogamy 
but  of  parthenogenesis,  since  the  synergid  is  to  be  regarded  as  a 
non-functioning  egg.  This  simply  serves  to  illustrate  the  fact 
that  categories  are  essentially  arbitrary  and  artificial.  A  third 
category  includes  those  cases  in  which  embryos  are  produced  by 
the  tissue  of  the  nucellus  or  of  the  integument.  This  is  not 
apogamy,  although  it  has  often  been  so  called,  for  it  is  a  case  in 
which  a  sporophyte  is  produced  by  sporophytic  tissue,  and  can 
be  included  under  the  general  name  of  budding.  In  addition 
to  the  normal  method,  therefore,  embryos  appear  among  Angio- 
sperms  in  three  ways,  namely,  by  parthenogenesis,  by  vegetative 
apogamy,  and  by  budding.  In  most  cases  vegetative  apogamy 
and  budding  are  associated  with  polyembryony,  and  they  will 
be  considered  under  that  head.  The  three  well-authenticated 
cases  of  parthenogenesis  among  Angiosperms  are  as  follows: 


THE  EMBRYO  211 

In  1898  Juel  53>  66  reported  parthenogenesis  in  Antennaria 
alpina,  and  two  years  later  published  a  very  full  account  of 
this  species  and  also  of  A.  dioica,  in  the  latter  of  which  fertili- 
zation occurs  regularly.  In  the  parthenogenetic  A.  alpitia  usu- 
ally only  pistillate  plants  are  found,  and  in  the  staminate  plants 
that  do  occur  the  pollen  is  either  lacking  or  feebly  developed. 
Juel  was  able  to  show  conclusively  that  the  embryo  develops 
from  the  unfertilized  egg.  He  was  also  able  to  satisfy  himself 
that  the  number  of  chromosomes  (about  fifty)  remains  un- 
changed throughout  the  entire  life  history,  no  reduction  taking 
place  in  the  formation  or  germination  of  the  megaspore.  The 
first  division  of  the  nucleus  of  the  megaspore  mother-cell  is  like 
the  divisions  in  vegetative  cells,  and  neither  in  the  form  of 
chromosomes  nor  in  the  character  of  the  spindle  does  it  resemble 
the  heterotypic  division  that  is  so  constantly  associated  with  the 
reduction  of  chromosomes.  The  mother-cell  gives  rise  to  only 
one  megaspore,  not  forming  a  tetrad.  In  A.  dioica,  in  which 
fertilization  regularly  occurs,  the  megaspore  mother-cell  gives 
rise  to  a  tetrad,  the  first  division  being  accompanied  by  a  reduc- 
tion in  the  number  of  chromosomes  (from  about  twenty-four  to 
about  twelve).  While  the  number  of  chromosomes  was  not  de- 
termined with  absolute  accuracy  for  either  species,  the  numer- 
ous countings  prove  the  principal  point,  namely,  that  in  A. 
dioica  a  reduction  occurs  at  the  beginning  of  the  gametophyte 
generation,  but  in  the  parthenogenetic  A.  alpina  the  number 
remains  unchanged  throughout  the  life  history.  In  the  latter 
also  the  polar  nuclei  do  not  fuse  to  form  a  primary  endosperm 
nucleus,  but  each  divides  independently  and  forms  a  mass  of 
endosperm,  showing,  like  the  egg,  an  ability  to  divide  without 
previous  fusion. 

In  1001  Murbeck  76  discovered  that  parthenogenesis  is  more 
or  less  constant  in  all  the  species  of  Alchemilla  belonging  to 
EUALCHEMILLA  ;  but  he  succeeded  in  finding  a  species  (A.  Ctr- 
l'ens  is)  in  which  fertilization  regularly  occurs.  In  the  struc- 
ture of  the  nucellus  AlcliemiUa  differs  decidedly  from  Anten- 
naria, there  being  a  large  number  of  megaspore  mother-cells, 
many  of  which  form  tetrads ;  and  it  is  not  uncommon  for  sev- 
eral of  the  resulting  megaspores  to  germinate.  The  general 
appearance  of  the  embryo-sac  is  normal,  and  the  polar  nuclei 
usually  fuse  to  form  a  primary  endosperm  nucleus.  Since  this 


212  MORPHOLOGY  OF  ANGIOSPERMS 

fusion  was  observed  in  several  parthenogenetic  species  of  Al- 
chemilla  (A.  sericata,  A.  "  hybrida"  A.  pubescens,  A.  pasto- 
raliSj  A.  acutangula,  A.  alpestris,  and  A.  speciosa),  its  failure, 
as  in  Antennaria  alpina,  can  hardly  be  regarded  as  character- 
istic of  parthenogenetic  forms.  In  the  parthenogenetic  species 
of  Alchemilla,  as  Antennaria  alpina,  the  number  of  chromo- 
somes remains  unchanged  throughout  the  life-history.  Al- 
though the  number  was  not  positively  established,  the  counting 
never  showed  less  than  thirty-two  or  more  than  forty-eight. 
In  Alchemilla  arvensis,  in  which  fertilization  regularly  occurs, 
the  numbers  are  sixteen  and  thirty-two.  Aside  from  the  more 
difficult  cytological  evidence,  a  convincing  proof  of  the  existence 
of  parthenogenesis  in  Alchemilla  alpina  is  found  in  the  fact 
that  the  segmenting  embryos  are  often  obtained  from  unopened 
buds  in  which  no  pollen  has  been  developed..  In  A.  arvensis 
(Murbeck77),  in  which  fertilization  occurs,  the  pollen-tube  en- 
ters the  chalaza  and  traverses  the  integument. 

In  1902  Overton 83  discovered  parthenogenesis  in  Thalic- 
trum  purpurascens,  the  investigation  having  been  suggested  by 
an  early  observation  that  Thalictrum  Fendleri  set  seed  freely 
in  the  absence  of  staminate  plants.  Only  ovulate  plants  were 
brought  into  the  greenhouse  and  forced.  These  set  seed  con- 
taining good  embryos  several  weeks  before  the  staminate  plants 
of  the  vicinity  had  developed  pollen.  Investigation  showed 
beyond  a  peradventure  that  these  embryos  were  derived  from 
unfertilized  eggs.  He  also  compared  normal  and  parthenoge- 
netic embryos,  and  found  that  the  latter  are  noticeably  slower 
in  starting,  though  the  two  kinds  become  exactly  alike  at  matu- 
rity. The  cytoplasm  is  very  dense  about  the  unfertilized  egg, 
and  wThen  a  zone  in  contact  with  the  egg  changes  in  appear- 
ance the  first  segmentation  occurs.  He  suggests  that  there  is 
a  reaction  of  some  kind  between  the  egg  and  the  contiguous 
cytoplasm  that  brings  about  the  change  in  the  physical  con- 
stitution of  the  egg  that  induces  segmentation.  This  is  con- 
ceivable from  the  fact  that  artificial  parthenogenesis  has  been 
induced  in  the  unfertilized  eggs  of  certain  low  animals  by 
changing  the  osmotic  pressure.  Overton  finds  that  in  nature 
this  species  probably  produces  normal  and  parthenogenetic  em- 
bryos in  about  equal  numbers. 

Still  more  recently  Treub  92  has  concluded  that  Ficus  hirta 


THE  EMBRYO  213 

produces  parthenogenetic  embryos.  The  observation  was  not 
direct  or  conclusive,  the  inference  being  based  upon  the  failure 
to  discover  pollen-tubes  although  embryos  were  common,  the 
feeble  development  of  endosperm,  and  the  poorly  developed 
synergids,  all  of  which  is  negative  evidence.  Treub  suggests 
that  the  stimulus  that  induces  the  egg  to  divide  in  this  case 
is  the  puncture  made  by  the  pollinating  wasp  Blastopliaga. 

There  seems  to  be  no  doubt  that  other  cases  of  partheno- 
genesis will  be  discovered  among  Angiosperms,  and  that  many 
embryos  supposed  to  be  normal  are  parthenogenetic.  There 
seems  to  be  no  reason  to  doubt  that  if  an  envelop  of  cytoplasm 
may  result  in  the  segmentation  of  the  egg  in  Thalictrum,  it  may 
often  have  the  same  result  in  other  cases.  For  example, 
Treub25  observed  that  in  certain  Burmanniaceae  (Gonyanthes 
Candida  and  Burmannia  javanica)  the  egg  does  not  segment 
until  the  embryo-sac  is  packed  full  of  endosperm.  Such  a  con- 
dition might  well  repeat  the  results  in  Thalictrum.  In  fact, 
all  cases  in  which  there  is  a  long  delay  before  the  egg  segments 
may  be  suspected  of  occasional  parthenogenesis. 

POLYEMBRYOXY 

Polyembryony  in  Angiosperms,  while  not  so  prevalent  as  in 
Gymnosperms,  is  by  no  means  a  rare  or  recently  discovered 
phenomenon.  As  early  as  1719,  Leeuwenhoek  found  two  em- 
bryos in  orange  seeds.  In  Euonymous  latifolius  polyembryony 
was  discovered  three  times  independently ;  by  Petit-Thouars  in 
1807,  by  Grebel  in  1820,  and  by  Treviranus  in  1838.  In  this 
species  about  one-half  of  the  ripe  seeds  are  said  to  contain  more 
than  one  embryo.  A.  Braun  in  1859  gave  an  historical  resume 
of  the  subject,  and  cited  sixty  cases  as  known  at  that  time. 
The  first  demonstration  of  the  real  nature  of  certain  cases  of 
polyembryony  was  made  by  Strasburger 12>  16  in  1878.  He 
found  that  in  Funkia  ovata,  Noilioscordon  fragrans,  Citrus 
Aurantium,  and  Coelebogyne  iUcifolia  the  cells  of  the  nucellus 
above  the  apex  of  the  embryo-sac  become  rich  in  contents,  divide 
and  grow,  and  form  several  embryos  that  push  the  sac  wall 
before  them  and  become  placed  in  the  seed  like  normal  em- 
bryos. In  Fun~ki&  the  egg  is  fertilized,  but  seldom  or  perhaps 
never  produces  an  embryo,  dividing  a  few  times  and  then  disor- 
ganizing (Fig.  99).  When  pollination  is  prevented  artificially, 


MORPHOLOGY   OF   ANGIOSPERMS 


FIG.  M.—Funkia  ovata,  showing  adventitious  embryos ;  fer- 
tilized egg  has  given  rise  to  weak  proembryo  of  three 
cells:  x  190.— 


the  adventitious  embryos  begin  to  develop  but  never  mature.    In 
Citrus  the  embryos  are  derived  not  only  from  the  cells  of  the 

nucellus  capping 
the  sac,  but  also 
from  those  lower 
down,  wrhich  may 
be  separated  from 
the  sac  by  several 
cells.  In  Coele- 
bogyne,  long  sup- 
posed to  be  par- 
thenogenetic,  fer- 
tilization never 
occurs  in  Europe, 
since  only  pistil- 
late plants  are 
cultivated.  These 

are  not  cases  of  apogamy,  as  often  stated,  but  are  evidently 
cases  of  vegetative  multiplication  or  budding,  since  the  em- 
bryos arise  from  sporophytic  tissue.  In  Opuntia  vulgaris 
(Ganong49)  the  ripe  seed  contains  one  large  embryo  and  sev- 
eral smaller  ones  pressed  to  one  side.  Half  ripe  seeds  generally 
show  that  the  large  embryo  comes  from  the  micropylar  end  of 
the  sac,  while  the  small  ones  arise  from  nucellar  tissue.  Among 
Cactaceae  the  only  previously 
known  case  of  polyembryony  is 
that  of  Opuntia  tortispina. 

The  multiplication  of  em- 
bryos by  budding  from  a  mass- 
ive suspensor  also  occurs,  and 
is  especially  common  in  the 
Lilium  type  of  embryogeny,  in 
which  the  suspensor  is  strongly 
meristematic.  In  1895  Jef- 
frey 35  called  attention  to  the 
fact  that  in  Erythronium  ameri- 
canum  the  suspensor  is  a  mass- 
ive and  lobed  tissue  on  whose 
free  surface  two  to  four  embryos  appear,  only  one  persisting 
(Fig.  100).  As  in  Funkia,  the  cells  of  the  nucellus  are 


FIG.  100.  —  Erythronium  americanum . 
Four  embryos  derived  from  fertilized 
egg ;  x  144.— .After  JEFFREY.85 


THE  EMBRYO 


215 


rich  in  protoplasmic  contents,  and  this  led  Jeffrey  to  sus- 
pect that  a  reinvestigation  of  Funkia  with  the  aid  of  modern 
technique  would  reveal  a  similar  condition.  The  examination, 
however,  confirmed  Strasburger's  account,  so  that  while  the 
general  appearance  of  sections  is  much  the  same  in  the  two 
(cf.  Figs.  99  and  100),  it  is  established  that  in  Funkia 
the  embryos  come  from  the  nucellus,  while  in  Erythronium  they 
come  from  the  fertilized  egg.  In  Erythronium  albidum  Schaff- 


em 


e  m 


D 


C 


FIG.  101. — Limnocharis  emarginata.  A-C,  three  sections  of  one  embryo,  showing  em- 
bryo proper  (e)  and  embryo-buds  from  suspensor  (em) ;  Z>,  appearance  of  growing 
point  of  stem  (gp). — After  HALL.82 

ner 72  found  the  same  large,  irregular,  and  much-lobed  sus- 
pensor, but  it  was  associated  with  only  one  embryo.  In  Tulipa 
Gesneriana  Ernst  69  also  observed  the  phenomenon  of  a  massive 
suspensor  associated  with  one  to  six  embryos,  only  one  of  which 
usually  persists.  In  these  cases  the  Lili-um  type  of  embryogeny 
is  obscured  by  the  early  and  rapid  growth  of  the  suspensor 
region  of  the  proembryo,  the  embryonal  cell  appearing  hardly 
more  than  one  of  the  cells  of  its  free  surface.  In  these  cases 
15 


216 


MORPHOLOGY  OF  ANGIOSPERMS 


of  polyembryony,  therefore,  one  of  the  embryos  is  to  be  regard- 
ed as  normal,  and  the  others  as  secondary  or  adventitious.     Ex- 
actly the  same  thing  sometimes  occurs  in  Limnocharis  emargir 
nata,  one  of  the  Alismaceae,  as  observed  by  Hall82  (Fig.  101). 
In  this  species  the  basal  suspensor-cell  may 
increase  very  much  in  size  and  remain  un- 
divided, as  is  most  common  in  the  Alisma 
type;  or  it  may  divide  extensively,  forming 
a  massive  tissue  from  which  several  embryos 
bud.      It  was   not   observed  whether   more 
FIG.  102.— Mimosa  Den-    than  one  embryo  matures,  but  presumably 
hartu.  Three  embryos    not.     This  case  is  interesting  not  only  on 
occupying  position  of   accmmt  of  the  polyembryony,  but  also  be- 

egg-apparatus  ;   x  384.  .  •  i  i      •        i 

—After  GUIOXARD."      cause  it  emphasizes  the  relation  between  the 

Alisma  and  Lilium  types  of  embryogeny. 
Illustrations  of  ordinary  apogamy  are  relatively  numerous, 
apparently  every  cell  within  the  embryo-sac  being  able  under 
certain  conditions  to  produce  an  embryo.  In  some  cases  a 
synergid  is  fertilized,  and  then  the  resulting  embryo  should 
probably  be  regarded  as  normal ;  it  certainly  is  not  apogamous. 
For  example,  Schwere 40  discovered 
synergid  fertilization  in  Taraxacum 
officinale ;  and  Guignard 68  has  ob- 
served that  in  Naias  major  the  per- 
sistent synergid  instead  of  the  pri- 
mary endosperm  nucleus  may  be  fer- 
tilized by  the  second  male  nucleus, 
resulting  in  two  embryos  lying  side 
by  side  (Fig.  103).  An  embryo  from 
a  synergid  in  addition  to  a  normal 
embryo  from  the  egg  has  been  re- 
ported by  several  observers.  In  Mi- 
mosa Denhartii  Guignard  21  has  found 
cases  which  suggest  the  development 
of  embryos  from  all  three  cells  of  the 
egg-apparatus.  Sometimes  two  simi- 
lar embryos  appear,  ono  in  the  position  of  the  egg  and  the 
other  in  that  of  a  synergid;  sometimes  a  group  occurred  con- 
sisting of  one  unchanged  synergid,  one  embryo  in  the  egg 
position,  and  a  second  embryo  in  the  position  of  the  second 


FIG.  103.  —  Set i as  major.  Two 
embryos,  one  from  fertilized 
egg,  the  other  from  fertilized 
synergid,  a  male  nucleus  hav- 
ing fused  with  nucleus  of 
synergid  instead  of  polar  nu- 
cleus ;  e,  endosperm  nucleus  ; 
x  176.— After  GITIGXABD." 


THE  EMBRYO  217 

synergid;  and  in  one  case  three  embryos  were  seen  occupying 
the  position  of  the  egg-apparatus  (Fig.  102).  Although  favor- 
ing this  interpretation,  Guignard  mentions  the  possibility  that 
the  extra  embryos  may  have  come  from  the  separation  of  early 
segments  of  the  egg.  a  view  doubtless  suggested  by  the  separa- 
tion of  the  cells  of  the  suspensor  in  certain  of  the  Legu- 
minosae. 

In  Vincetoxicum  nig  rum  and  V.  medium  Chauveaud 33 
finds  that  polyembryony  is  a  regular  phenomenon,  one,  two, 
three,  four,  and  even  five  embryos  appearing,  more  than  one 
of  which  may  reach  maturity.  The  synergids  are  doubtless 
involved.  Chauveaud  found  four  or  five  bodies  in  the  pollen- 
tube  which  he  thought  might  be  interpreted  as  male  nuclei,  and 
responsible  for  polyembryony.  He  also  concludes  that  poly- 
embryony is  a  primitive  feature  of  Angiosperms,  the  number 
having  been  reduced  in  the  interest  of  one  strong  embryo.  In 
describing  synergid  fertilization  in  Iris  sibirica,  Dodel 31  im- 
plies a  somewhat  similar  view,  when  he  interprets  the  synergids 
as  partially  aborted  eggs.  In  this  form  more  than  one  pollen- 
tube  may  enter  the  rnicropyle. 

In  certain  orchids,  as  Gymnadenia  conopsea  (Stras- 
burger16),  two  embryos  sometime  occur  in  the  same  sac,  but 
their  origin  is  uncertain,  although  it  is  very  probable  that  one 
of  them  is  derived  from  a  synergid,  either  apogamously  or  by 
fertilization. 

In  a  preliminary  paper,  Hegelmaier  79  states  that  polyem- 
bryony is  habitual  in  Euphorbia  dulcis,  two  to  nine  embryos 
appearing  at  the  micropylar  end  of  the  sac.  One  of  the  em- 
bryos, which  certainly  comes  from  the  egg  and  may  be  dis- 
tinguished from  the  others  by  the  presence  of  a  suspensor, 
becomes  the  functional  embryo.  Fertilization  was  not  studied, 
and  so  the  origin  of  some  of  the  embryos  is  in  doubt,  although 
it  is  certain  that  some  come  from  the  nucellus.  Two  embryos 
often  reach  the  cotyledon  stage,  with  tissue  systems  differen- 
tiated, while  the  others  appear  as  irregular  masses. 

Allium  odor  urn  presents  a  remarkable  case  of  polyembryony. 
In  1895  Tretjakow36  reported  one  to  three  embryos  from  the 
antipodal  cells  (Fig.  104),  the  fertilized  egg  and  sometimes  a 
synergid  forming  additional  embryos.  In  the  same  species 
Hegelmaier 45  observed  five  embryos  in  a  single  embryo-sac ; 


218 


MORPHOLOGY  OF  ANGIOSPERMS 


one  normal,  one  from  a  synergid,  two  from  antipodal  ceils,  and 
one  from  the  inner  integument  (Fig.  105).  It  is  interesting 
to  note  that  while  polyembryony  is  so  frequent  in  Allium  odo- 
rum,  it  has  not  been  observed  in  other 
species  of  the  genus.  JEegelmaier  exam- 
ined A.  fistulosum  and  A.  ursinum,  and 
Elmore  50  made  a  thorough  study  of  A. 
cernuum,  A.  tricoccum,  and  A.  canadense, 
without  discovering  a  single  extra  em- 
bryo, reporting  also  very  small  and  eva- 
nescent antipoclals.  In  parthenogenetic 
species  of  AlchemiUa  Murbeck76  found 
embryos  from  the  egg,  from  the  synergids, 
from  the  three  antipo-  and  from  the  nucellar  tissue  (Fig.  106). 

In  Balanophora  elongata  and  B.  glo- 
bosa  fertilization  is  known  not  to  occur, 
and  both  Treub  46  and  Lotsy  58  state  that  the  embryo  is  formed 
by  the  upper  polar  nucleus.  In  addition  to  this,  a  cell  in  the 
midst  of  the  endosperm  is  said  to  develop  into  a  five  to  ten- 
celled  "  pseud-embryo/'  whose  significance  and  history  we  are 


dal   cells;    x  116.— After 

TRETJAKOW.36 


FIG.  105. — Allium  odorum.  A,  section  of  ovule  with  four  embryos,  one  from  egg.  one 
from  a  synergid,  ore  from  an  antipodal  cell,  and  one  from  the  Avail ;  x  15 ;  J2,  tAvo 
embryos,  one  from  egg  and  one  from  a  synergid:  the  other  synergid  someAvhat 
enlarged  and  lying  between  the  two  embryos ;  x  246  ;  (7,  embryo  derived  from  inner 
integument :  *,  inner  integument ;  o,  outer  integument ;  x  246. — After  HEGELMAiER.46 

at  a  loss  to  understand  (Fig.  107).  In  the  allied  Helosis  guaya- 
nensis,  also,  Chodat  and  Bernard  64  think  that  fertilization  does 
not  occur,  and  that  the  embryo  arises  apogamously  from  the 
endosperm. 

It  is  evident  that  polyembryony  is  by  no  means  so  rare  a 


THE  EMBRYO 


219 


phenomenon  as  many  may  have  supposed.  The  cases  on  record 
are  already  so  numerous  that  only  an  exhaustive  study  of  the 
literature  would  make  it  safe  to  venture  an  estimate  of  the 
number.  Since  in  nearly  all  the  cases  described  this  phenome- 
non is  rare  rather  than  habitual,  it  is  probable  that  under  con- 
ditions not  yet  understood  a  large  number  of  plants  may  exhibit 
polyembryony  occasionally. 


FIG.  106. — Embryos  in  parthenogenetic  species  of  Alchemilla.  A,  A.  sericata,  one  par- 
thenogenetic embryo  from  egg  and  one  from  synergid,  the  other  synergid  breaking 
down;  the  two  polar  nuclei  and  antipodal  cells  also  shown:  x  284;  .Z?,  A.  pastoralis, 
showing  one  synergid  partly  disorganized,  one  embryo  of  four  cells  from  unfertilized 
esrir,  one  embryo  from  nucellus,  two  polar  nuclei  and  one  synergid  nucleus  forming 
group  at  middle  of  sac,  also  three  disorganizing  antipodal  cells;  x  190.  After 

MURBECK.80 


The  scattered  literature  of  the  subject  is  admirably  sum- 
marized by  Ernst  69  in  his  presentation  of  polyembryony  in 
TuUpa  Gesneriana.  The  following  synoptical  statement  is 
taken  from  Ernst,  and  supplemented  by  the  more  recent  addi- 
tions. Tn  case  the  same  form  is  treated  in  several  accounts, 
there  is  no  attempt  to  cite  all  of  them  or  even  the  first  refer- 
ence, but  a  selection  is  made  of  those  citations  that  direct  to 


FIG.  107. —  Balanophora  elongata.  Stages  in  development  of  embryo-sac,  endosperm, 
and  embryo.  A,  archegonium-like  megasporangium  with  mother-cell  that  becomes 
megaspore  directly  without  forming  tetrad ;  x  145 ;  -B,  quadrinucleate  stage  of 
embryo-sac;  x  200;  (7,  nearly  mature  sac  showing  above  the  two  synergids  and 
oosphere,  just  beneath  the  micropylar  polar  nucleus,  and  at  opposite  end  of  sac  a 
group  of  four  nuclei,  the  three  antipodals,  and  the  lower  polar  nucleus;  x  280;  Z>, 
at  upper  end  the  synergids  and  egg  are  disorganizing,  just  beneath  are  two  cells 
resulting  from  first  division  of  upper  polar  nucleus  ;  x  280  ;  E,  six  cells  of  endosperm 
shown;  syuergids  and  egg  still  visible  at  upper  end  of  sac;  x  300;  F,  two-celled 
embryo  formed  from  an  inner  cell  of  the  endosperm  ;  x  300. — 
220 


THE  EMBRYO  221 

the  most  complete  descriptions.  The  forms  that  Ernst  includes 
under  "  pseudo-polyembryony  "  are  not  treated  in  our  discus- 
sion of  the  subject. 

Pseudo-poly  embryony. 

1.  OVULES   GROWN  TOGETHER.    Pirus  Mains,  Loranthus  euro- 
paeus.  Viscum  album  (all  A.  Braun4). 

2.  DIVISION    OF    NUCELLUS.     Morns  albus  (Hofmeister2).   Orchis 
Morio  (Braun4),  Gymnadenia  conopsea  (Strasburger16),  Coffea  ara- 
bica  (Hanausek  "). 

<-  3.  DEVELOPMENT  OF  SEVERAL  EMBRYO  SACS  IN  THE  SAME  NU- 
CELLUS. Cheiranthus  Cheiri  (Schacht3),  Rosa  sp.  (Hofmeister2), 
Rosa  livida  (Strasburger12),  Trifolium  pratense  (Jonsson23),  Taraxa- 
cum officinale  (Schwere40). 

True  Poly  embryony. 

A.  Embryos  derived  from  cells  outside  the  sac,  hence  from  sporo- 
phytic  tissue  (vegetative  multiplication  or  budding). 

1.  EMBRYOS  DERIVED  FROM  CELLS  OF  THE  NUCELLUS.    Funkia 
ovata  (Strasburger12),  Nothoscordon  fragrans  (Strasburger12),  Citrus 
Aurantium  (Strasburger 16),  Mangifera  indica  (Strasburger  ").  Euony- 
mus    americanus   (Braun4),    Coelebogyne   ilicifolia   (Braun.4  Stras- 
burger16), Clusia  alba  (Goebel 67),  Opuntia  vulgaris  (Ganong49),  Al- 
chemilla  pastoralis  (Murbeck90). 

2.  EMBRYOS  FROM  CELLS  OF  THE  INTEGUMENT.    Allium  odorum 
(Tretjakow,36  Hegelmaier 46). 

B.  Embryos   derived  from  cells  within  the  sac  (parthenogenesis 
and  vegetative  apogamy)  ;  although  not  in  the  same  morphological 
category,  embryos  from  the  suspensor  are  also  included  in  the  list 
(vegetative  multiplication  or  budding). 

1.  NORMAL   OCCURRENCE   OF  Two  EGGS.    Santalum  album  and 
Sinningia  Lindleyana  (both  Strasburger 12). 

2.  EMBRYOS  FROM  SYNERGIDS.    Glaucium  luteum  (Hegelmaier13), 
Mimosa  Denhartii  and  Schrankia  uncinata  (Guignard21j,  Iris  sibi- 
rica  (Dodel?1),  Lilium  Martagon  (Overton"),  Vincetoxicum  nigrum 
and  V.  medium  (Chauveaud 33),  Allium  odorum  (Tretjakow,36  Hegel- 
maier45).   Taraxacum    officinale    (Schwere40),   Aconitum    Napellus 
(Osterwalder52),    AlchemiUa     sericata     (Murbeck90),    Naias    major 
(Guignard  68). 

3.  SPLITTING  OF  EMBRYO  DERIVED  FROM  EGG.    Loranthus  euro- 
paeus  (Braun  *). 

4.  EMBRYOS  FROM   ANTIPODAL   CELLS.    Allium  odorum  (Tretja- 
kow.38 Hegelmaier13). 

5.  EMBRYOS    FROM    ENDOSPERM    CELLS.    Balanopliora  elongata 
(Treub49). 


222  MORPHOLOGY  OF  ANGIOSPERMS 

6.  EMBRYOS  FROM  THE  SUSPENSOR.  Erythronium  dens-canis 
(Hofmeister 6),  E.  americanum  (Jeffrey86),  Tulipa  Gesneriana 
(Ernst69),  Limnocharis  emarginata  (Hall82). 

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224  MORPHOLOGY  OF  ANGIOSPERMS 

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Mem.  Torr.  Bot.  Club  8:  27-112.  pis.  5-15.  1902. 

86.  JOHNSON,  D.  S.     On  the  Development  of  Certain  Piperaceae.     Bot. 

Gazette  34:  321-340.  pis.  9-10.  1902. 

87.  PECHOUTRE,   F.     Contribution    a  1'etude  du    developpement    de 

Tovule  et  de  le  graine  des  Rosacees.  Ann.  Sci.  Nat.  Bot.  VIII. 
16:  1-158.  figs.  166.  1902. 

88.  LYON,  H.  L.     The  Phylogeny  of  the  Cotyledon.    Postelsia  1901 : 

55-86.  1902. 

89.  SARGANT,  ETHEL.    The  Origin  of  the  Seed-leaf  in  Monocotyledons. 

The  New  Phytologist  1 :  107-113.  pi.  2.  1902. 

90.  MURBECK,  S.    Ueber  Anomalien  im  Baue  des  Nucellus  und  des- 

Embryosackes  bei  partheiiogenetischen  Arten  der  Gattung  Al- 
chemilla.  Lunds  Univ.  Arsskrift  383 :  no.  2.  pp.  10.  pis.  13. 
1902. 

91.  SCHMID,  B.     Beitrage  zur  Embryo-Entwickelung  einiger  Dicotylen, 

Bot.  Zeit.  60 :  207-230.  pis.  8-10.  1902. 

92.  TREUB,   M.      L'organe  femelle  et  1'embryogenese  dans  le  Ficus 

hirta  Vahl.  Ann.  Jard.  Bot.  Buitenzorg  II.  3 :  124-157.  pis.  16- 
25.  1902. 

93.  JUEL,  H.  O.     Zur  Entwicklungsgeschichte  des  Samens  von  Cyno- 

morium.     Beih.  Bot.  Centralbl.  13  :  194-202.  Jigs.  5.  1902. 

94.  SARGANT,  ETHEL.    A  Theory  of  the  Origin  of  Monocotyledons, 

founded  on  the  Structure  of  their  Seedlings.  Annals  of  Botany 
17:  1-92.  pis.  1-7.  1903. 

95.  MURBECK,   S.     Ueber  die   Embryologie  von   Ruppia  rostellata- 

Koch.     Handl.  Svensk.  Yetensk.  Akad.  36 :  pp.  21.  pis.  3.  1902. 


CHAPTER    X 

CLASSIFICATION   OF   MONOCOTYLEDONS 

A  SATISFACTORY  classification  of  Angiosperms  still  remains 
an  impossible  task.  The  immense  number  of  species  and  their 
entanglement  of  relationships,  as  well  as  our  merely  superficial 
knowledge  of  the  great  majority  of  forms,  have  made  progress 
toward  a  natural  classification  very  slow.  Since  the  time  of 
John  Ray  (1703)  steps  in  this  progress  have  been  taken  by 
De  Jussieu  (1789),  De  Candolle  (1819),  Endlicher  (1836- 
1>40')?  Brongniart  (1843),  Braun  (1864),  Bentham  and 
Hooker  (1862-1883),  Eichler  (1883),  Engler  (1892),  and 
others.  Xaturally,  the  increasing  knowledge  of  morphology 
and  the  changed  conception  of  species  have  gradually  broken 
up  artificial  assemblages,  but  much  of  classification  is  still  arti- 
ficial. It  does  not  lie  within  the  purpose  of  this  book  to  trace 
the  historical  development  of  classification,  nor  to  present  an- 
other scheme  for  consideration.  We  merely  adopt  the  classi- 
fication of  Eichler  as  modified  by  Engler,  and  elaborated  in 
Engler  and  Fraud's  Die  Natiirliclien  Pflanzenfamilien,  as  the 
best  expression  of  our  present  knowledge  of  morphology  as 
applied  to  the  whole  of  Angiosperms.  The  special  student  of 
morphology  must  have  enough  knowledge  of  general  relation- 
ships to  enable  him  to  select  critical  forms  for  investigation  and 
to  appreciate  the  bearings  of  his  results.  The  purpose  of  the 
following  presentation,  therefore,  is  to  trace  in  a  general  way 
the  evolution  of  Angiosperms  and  to  point  out  the  greatest  gaps 
in  knowledge,  using  the  classification  mentioned  as  the  best 
available  basis.  Xo  attempt  is  made  to  use  the  varying  termi- 
nology of  the  larger  groups  of  classification,  but  coordinate 
groups  are  indicated  by  common  endings. 

According  to  Engler,  the  general  tendency  among  Monocot- 

227 


228  MORPHOLOGY  OF  ANGIOSPERMS 

yledons  is  to  advance  from  naked  flowers  with  parts  spirally 
arranged  and  indefinite  in  number  to  peiitacyclic  trimerous 
flowers.  There  are  also  such  lines  of  advance  as  from  apocarpy 
to  syncarpy,  from  hypogyny  to  epigyny,  from  actinomorphy 
to  zygomorphy,  etc.  These  tendencies  are  often  very  unequally 
expressed  even  by  different  groups  of  the  same  alliance,  one 
group  developing  chiefly  along  one  line,  and  another  group 
along  another  line,  so  that  the  results  are  very  different.  It  is 
also  often  a  question  whether  a  simple  floral  structure  is  primi- 
tive or  reduced.  In  the  older  morphology  there  was  a  typical 
floral  structure,  and  all  simpler  ones  were  regarded  as  reduced 
forms.  There  can  be  no  doubt  that  there  are  reduced  floral 
structures,  as  in  Lemna;  but  the  great  majority  of  simple 
flowers  are  probably  primitive. 

Upon  these  and  other  considerations,  Engler  has  subdivided 
the  Monocotyledons  into  ten  great  alliances.  The  first  six  con- 
stitute the  more  primitive  Spiral  series,  and  although  the  trim- 
erous habit  appears  among  them,  the  spiral  arrangement  and 
indefinite  numbers  occur  in  one  or  more  sets.  The  remaining 
four  -alliances  constitute  the  Cyclic  series,  the  highly  specialized 
Monocotyledons. 

I.  PANDANALES. — This  includes  the  Pandanaceae,  Typha- 
ceae,  and  Sparganiaceae,  together  containing  a  little  more  than 
100  species.  The  Pandanaceae  (about  80  species),  or  screw- 
pines,  belong  to  the  oriental  tropics,  chiefly  the  coasts  and  is- 
lands of  the  Indian  and  Pacific  oceans ;  while  the  other  families 
are  mainly  represented  in  temperate  regions. 

That  these  forms  are  primitive  Monocotyledons  is  indicated 
by  the  following  facts :  there  is  nothing  to  represent  a  perianth 
unless  the  floral  bracts  of  Sparganium  be  regarded  as  one ;  the 
sporophylls  are  mostly  spiral  and  indefinite  in  number,  the  sta- 
mens of  Pandanaceae  often  being  very  numerous  and  exhibiting 
the  greatest  variation  in  arrangement ;  the  species  are  all  hydro- 
phytic ;  and  the  plants  are  anemophilous.  Such  flowers  as  those 
of  the  Pandanaceae  and  Typhaceae  are  extremely  simple,  the 
peculiar  hairs  accompanying  the  sporophylls  of  the  latter  ap- 
parently representing  sterile  sporophylls ;  while  the  Spargania- 
ceae are  the  most  advanced  members  of  the  alliance,  a  perianth 
probably  being  represented  by  a  set  of  small  bracts,  and  the 
trimerous  character  appearing. 


CLASSIFICATION  OF  MONOCOTYLEDONS  229 

A  well-marked  feature  of  the  group  is  the  protection  of  the 
flower-clusters  by  a  prominent  leaf-sheath.  The  development 
of  this  sheath  as  a  protecting  organ  before  the  appearance  of  a 
fully  developed  perianth  is  one  of  the  constant  features  of  the 
more  primitive  Monocotyledons,  and  in  some  of  the  following 
groups  it  becomes  highly  specialized. 

The  hydrophytic  Pandanales,  therefore,  begin  in  the  great- 
est simplicity,  so  far  as  floral  structures  are  concerned,  the 
Pandanaceae  being  the  most  primitive  forms  on  account  of  the 
indefinite  number  of  the  sporophylls  and  the  spiral  arrangement 
of  the  stamens,  and  the  series  has  not  advanced  very  far.  It 
should  be  remembered,  however,  that  the  three  existing  families 
probably  represent  fragments  of  a  formerly  much  larger  alli- 
ance, so  that  the  association  of  the  temperate  Typha  and  Spar- 
(janium  with  the  tropical  Pandanaceae  may  not  be  so  unnatural 
in  reality  as  it  appears  at  present.  It  is  extremely  desirable  to 
obtain  some  accurate  knowledge  of  the  essential  morphology  of 
the  Pandanaceae. 

II.  HELOBIALES. — This  includes  the  Potamogetonaceae, 
Xaiadaceae,  Aponogetonaceae,  Juncaginaceae,  Alismaceae,  Bu- 
tomaceae,  and  Hydrocharitaceae,  together  containing  about  235 
species.  Engler  has  set  apart  the  small  family  Triuridaceae, 
containing  about  18  species,  as  representing  a  distinct  series, 
TBIURIDALES,  but  this  can  be  disregarded  in  this  very  general 
presentation. 

This  is  one  of  the  most  remarkable  of  the  monocotyledonous 
lines  in  its  extent,  reaching  from  the  greatest  floral  simplicity 
in  Potamogetonaceae  to  highly  developed  flowers  in  Hydro- 
charitaceae. It  has  been  called  an  unstable  or  plastic  line,  and 
may  have  given  rise  to  higher  forms ;  in  any  event  it  is  probably 
to  be  regarded  as  one  of  the  most  important  phylogenetic  lines 
among  the  Monocotyledons.  For  this  reason  morphological 
investigation  in  recent  years  has  specially  cultivated  this  series 
of  forms,  particularly  the  more  primitive  families.  About  the 
only  taxonomic  character  that  holds  these  diverse  forms  together 
is  the  fact  that  they  are  exceptional  among  Monocotyledons  in 
the  feeble  development  of  endosperm.  They  are  characteris- 
tically aquatic,  and  sheathing  bracts  enclosing  the  flower-clus- 
ters are  largely  developed.  In  most  of  the  forms  the  spiral 
arrangement  and  indefinite  number  of  floral  parts  is  very  appar- 


230  MORPHOLOGY  OF   AXGIOSPERMS 

ent,  but  the  line  -as  a  whole  presents  almost  a  complete  series 
from  the  simplest  floral  structure  to  one  of  the  most  highly 
developed. 

The  series  of  floral  changes  may  be  broadly  indicated  as 
follows.  In  Potamogetonaceae  and  ^Naiadaceae  there  is  no  peri- 
anth, and  the  stamens  and  carpels  are  indefinite  in  number ;  in 
Juncaginaceae  a  bract-like  perianth  is  present,  there  is  a  dis- 
tinct tendency  toward  the  trimerous  habit,  and  syncarpy  may 
occur;  in  Alismaceae  the  perianth  is  differentiated  into  calyx 
and  corolla,  and  the  trimerous  tendency  is  very  clear,  though 
the  carpels  are  usually  indefinite  in  number;  in  Hydrocharita- 
ceae,  in  addition  to  a  differentiated  perianth  and  a  strong  ex- 
pression of  the  trimerous  tendency  (although  the  stamens  and 
carpels  are  often  indefinite  in  number),  the  flowers  are  epigy- 
nous.  The  plants  are  chiefly  anemophilous  or  hydrophilous, 
but  the  appearance  of  a  differentiated  perianth  in  the  Alisma- 
ceae is  probably  associated  with  a  certain  amount  of  ento- 
mophily. 

Heliobales,  therefore,  begin  with  as  great  simplicity  of 
floral  structure  as  do  the  Pandanales,  but  they  have  advanced 
much  further  in  floral  development.  That  such  an  extensive 
line  comprises  so  few  species  is  probably  associated  with  the 
uniformity  of  aquatic  conditions.  In  the  whole  series,  how- 
ever, there  is  no  distinct  settling  into  a  complete  trimerous 
habit,  which  is  intimated  rather  than  established. 

III.  GLTJMALES.* — In  this  alliance  are  the  two  great  fami- 
lies Gramineae  and  Cyperaceae,  the  former  including  about 
351  genera  and  4,700  species,  the  latter  76  genera  and  about 
2,300  species.  In  point  of  species  this  is  one  of  the  greatest  of 
angiospermous  alliances,  and  in  display  of  individuals  it  is  un- 
questionably the  greatest.  The  common  features  of  the  two 
families  are  the  absence  of  a  perianth,  the  protection  of  the 
flowers  by  special  bracts,  the  fluctuating  of  the  stamens  between 
one  and  many,  the  solitary  carpel,  and  anemophily.  It  is  not 
probable  that  the  two  families  are  related  to  one  another  genet- 
ically, but  they  represent  approximately  the  same  stage  of  floral 
development. 

The  peculiar  features  of  the  bract-protection,  as  contrasted 

*  GLUMIFLORAE  of  Engler. 


CLASSIFICATION  OF  MONOCOTYLEDONS  231 

with  the  preceding  alliances,  is  that  the  bract  does  not  eusheath 
a  whole  flower-cluster  but  individual  flowers.  It  is  this  charac- 
teristic bract  (glume,  palet)  that  gives  name  to  the  alliance. 
The  lodicules  of  Gramineae  and  certain  hairs  and  bracts  of 
Cvperaceae  are  regarded  by  some  as  representing  a  perianth. 
Even  if  this  doubtful  claim  be  allowed,  such  a  perianth  is 
better  regarded  as  one  that  is  very  primitive  rather  than  re- 
duced. 

The  primitive  character  of  Glumales  is  indicated  by  the 
characters  given  above,  but  contrasted  with  the  Helobiales  it  is 
a  rigid  group  that  has  not  advanced  far  in  floral  development, 
but  has  proved  to  be  a  remarkably  successful  type  of  vegeta- 
tion. Moreover,  it  is  the  primitive  group  of  Monocotyledons 
that  seems  to  have  been  the  first  to  establish  itself  upon  the 
drier  and  more  diversified  land  surface,  and  this  fact  may  hold 
some  relation  to  its  structural  stability  and  its  great  display  of 
species.  Evidence  of  its  aquatic  origin  may  be  obtained  not 
only  from  the  numerous  hydrophytic  forms,  but  also  from  ana- 
tomical characters  that  relate  it  to  Helobiales  and  Pandanales 
rather  than  to  the  terrestrial  alliances. 

Pandanales,  Helobiales,  and  Glumales  are  the  only  three 
alliances  of  Monocotyledons  that  include  the  most  primitive 
type  of  monocotyledonous  floral  structure.  Their  possible  ge- 
netic relation  to  one  another  is  entirely  obscure,  and  in  their 
present  display  they  seem  to  emerge  from  the  beginnings  of  the 
history  of  Monocotyledons  as  independent  lines.  The  remain- 
ing seven  alliances  are  either  derived  from  these  three,  or  their 
primitive  members  have  disappeared. 

IV.  PALM  ALES.  * — The  palms  are  the  chief  representatives 
of  monocotyledonous  trees,  and  are  characteristic  of  all  tropical 
regions.  The  single  family  Palmaceae  includes  about  150  gen- 
era and  1,100  species,  though  these  numbers  will  doubtless  be 
much  increased  when  the  palms  are  studied  in  their  habitats. 
A  knowledge  of  the  essential  morphology  of  this  group  is  also 
much  to  be  desired. 

A  perianth  is  always  present,  although  it  is  very  "  rudimen- 
tary "  and  hence  doubtful  in  Phytelephas  and  Coryphanthe, 
but  it  is  not  differentiated  into  a  distinct  calvx  and  corolla. 


*  PRIXCIPES  of  Engler. 
16 


232  MORPHOLOGY  OF  ANGIOSPERMS 

As  there  are  no  naked  flowers,  this  group  does  not  have  as 
primitive  members  as  do  the  three  preceding  ones.  The  sta- 
mens are  extremely  variable  in  number,  ranging  from  three 
to  indefinitely  numerous,  showing  the  primitive  spiral  charac- 
ter; while  the  carpels  are  usually  three  and  sometimes  form  a 
syncarpous  pistil.  The  enormous  flowTer-cluster  is  ensheathed 
by  a  great  bract  (spathe)  that  is  more  or  less  tough  and  even 
woody,  a  feature  recalling  the  same  tendency  in  Pandanales 
and  Helobiales.  As  the  axis  of  inflorescence  is  sometimes 
thickened  and  the  flowers  more  or  less  embedded  in  it,  the 
inflorescence  is  often  spoken  of  as  a  branching  spadix. 

These  characters  indicate  a  group  as  a  whole  considerably 
further  advanced  than  the  preceding  ones  in  the  constant  pres- 
ence of  a  definite  perianth,  although  it  is  undifferentiated.  The 
association  of  floral  envelops  with  a  spathe  is  of  interest,  but 
in  such  conditions  a  highly  developed  perianth  could  not  be 
expected.  While  there  is  doubtless  anemophilous  pollination, 
entomophily  must  exist  to  a  certain  extent.  The  whole  struc- 
ture suggests  one  that  is  intermediate  between  the  dominance 
of  bract  and  perianth,  between  anemophily  and  entomophily. 

Palmales,  therefore,  differ  from  Glumales  in  the  definite 
trimerous  perianth,  as  well  as  in  numerous  other  features; 
from  the  Helobiales  in  that  the  number  of  carpels  is  constant ; 
biit  through  Phytelephas  and  Coryphanthe,  with  their  rudimen- 
tary perianth,  as  well  as  through  general  habit,  the  connection 
with  Pandanales  seems  clear.  It  seems  probable,  therefore, 
that  the  Palmales  have  been  derived  from  the  Pandanales,  sur- 
passing the  Glumales  in  floral  development,  but  not  reaching 
the  differentiation  of  calyx  and  corolla  and  epigyny  attained  by 
the  higher  members  of  the  Helobiales. 

\7.  SYNAETHAI/ES.* — This  includes  a  small  family  (Cy- 
clanthaceae)  of  the  American  tropics,  represented  by  about  45 
species,  and  usually  and  naturally  associated  with  the  screw- 
pines  and  palms.  The  flowers  are  in  an  unbranched  spadix, 
either  scattered  or  in  a  close  spiral,  and  there  is  generally  an 
evident  bract-like  perianth  in  one  or  two  cycles.  The  stamens 
range  from  six  to  indefinitely  numerous,  and  the  carpels  are 
one  to  four.  In  the  staminate  flowers  there  is  no  trace  of  car- 

*  SYNANTHAE  of  Engler. 


CLASSIFICATION  OF  MONOCOTYLEDONS  233 

pels  and  the  stamens  are  connate ;  while  in  the  carpellaie  flowers 
there  are  very  conspicuous  and  often  branching  staminodia. 
There  is  a  strong  tendency  to  "  coalescence  "  in  all  the  members, 
the  perianth  often  being  tubular,  the  stamens  usually  connate, 
and  the  carpels  (if  more  than  one)  always  forming  a' syncar- 
pous  pistil.  The  group  is  also  peculiar  in  the  very  numerous 
ovules  upon  a  single  parietal  placenta. 

Too  little  is  known  of  the  morphology  of  the  group  to  speak 
of  its  relationships  with  any  definiteness,  but  it  seems  safe  to 
regard  it  as  another  branch  of  the  Pandanales  stock.  The  Pan- 
danales, Pahnales,  and  Synanthales  are  thus  referred  to  a  com- 
mon origin,  with  the  Pandanales  as  the  most  primitive  repre- 
sentative of  the  stock.  This  tropical  association  seems  to  be  a 
strange  one  for  Typlia  and  Sparganium,  but  otherwise  it  seems 
to  be  entirely  natural,  and  not  clearly  related  to  any  other  Mono- 
cotyledons. 

VI.  ARALES.* — This  includes  the  Araceae  with  about  1,000 
species,  and  the  Lemnaceae  with  about  25.  The  Aroids  form 
one  of  the  most  distinct  and  also  diversified  groups  of  Monocot- 
yledons. The  characteristic  features  are  the  spadix,  the  highly 
developed  spathe,  and  the  broad  net-veined  leaves.  There  is 
also  probably  greater  anatomical  differentiation  than  in  any- 
other  monocotyledonous  group,  which  is  taken  advantage  of 
in  their  classification.  The  floral  structure  is  of  three  general 
types:  (1)  the  Calamus  type,  in  which  the  flowers  are  bisporan- 
giate,  pentacyclic,  2  to  4-merous,  and  syncarpous;  (2)  the  Calla 
type,  in  which  the  flowers  are  bisporangiate,  with  no  perianth, 
6  to  9  stamens,  and  1  carpel;  (3)  the  Arum-  type,  in  which 
the  flowers  are  monosporangiate  (staminate  flowers  above  and 
carpellate  flowers  below  on  the  same  spadix),  and  with  no 
perianth. 

It  is  evident  that  the  floral  structure  is  extremely  fluctua- 
ting, and  that  this  is  probably  associated  with  the  extreme  spe- 
cialization of  the  spathe.  Engler  has  called  attention  to  the 
fact  that  the  flowers  with  a  perianth  are  associated  with  a 
bract-like  spathe;  while  those  without  a  perianth  (the  great 
majority)  are  associated  with  a  petaloideous  spathe.  In  any 
event,  the  bract  reaches  its  highest  specialization  in  this  group, 

*  SPATHIFLORAE  of  Engler. 


234  MORPHOLOGY   OF  ANGIOSPERMS 

being  not  merely  a  protecting  organ,  but  immensely  varied  in 
form,  texture,  and  color  to  secure  entomophily.  '  In  other  words, 
the  conspicuous  function  of  the  perianth  in  the  petaloideous 
groups  is  here  assumed  by  the  spathe,  and  the  flowers  retain 
for  the  most  part  the  primitive  character. 

There  are  many  features  of  the  Aroids  that  suggest  the  He- 
lobiales,  especially  the  Potamogetonaceae,  so  that  Engler 
inclines  to  the  belief  that  they  have  been  derived  from  that 
stock.  If  this  be  true,  they  represent  a  strong  terrestrial  branch 
from  the  aquatic  Helobiales,  that  in  tropical  conditions  has 
become  extremely  varied  in  form  and  structure,  and  that  has 
assumed  the  erect,  climbing,  and  epiphytic  habits.  It  does  not 
seem  probable  that  any  other  monocotyledonous  alliance  is  asso- 
ciated with  these  two  in  origin;  but  the  suggestion  has  been 
made  that  from  the  Aroids  the  Dicotyledons,  or  at  least  some 
of  their  phyla,  may  have  been  derived.  One  of  the  most  prom- 
ising fields  of  morphological  research  is  among  the  tropical 
Aroids. 

The  Lemnaceae  represent  a  distinct  reduction  series,  being 
Aroids  adapted  to  the  free-swimming  habit,  and  remarkably 
reduced  in  structure,  Wolffia  being  the  smallest  known  seed- 
plant. 

The  six  great  alliances  just  considered  constitute  the  Spiral 
series  of  Engler,  with  inconstant  number  of  floral  members, 
with  mostly  no  perianth  or  one  not  adapted  to  entomophily, 
and  with  a  striking  development  of  sheathing  leaves  or  bracts 
in  connection  with  the  inflorescence  or  the  individual  flowers. 

The  four  remaining  alliances  constitute  the  Cyclic  series,  in 
which  the  almost  constant  floral  formula  is  perianth  3  +  3, 
stamens  3  -j-  3,  carpels  3  and  forming  a  syncarpous  pistil.  The 
two  perianth  sets  may  be  variously  modified,  but  there  runs 
through  the  series  an  increasing  specialization  of  the  perianth 
for  entomophily,  which  reaches  its  extreme  expression  in  the 
Orchidaceae.  As  a  consequence,  the  perianth  rather  than 
bracts  becomes  the  conspicuous  floral  feature.  The  pentacy- 
clic  trimerous  habit  having  become  established,  the  cyclic  groups 
have  largely  differentiated  in  the  direction  of  a  conspicuous 
perianth,  epigyny,  and  zygomorphy.  The  number  of  species 
involved  is  so  great  that  only  the  broadest  outlines  can  be  con- 
sidered. 


CLASSIFICATION  OF  MONOCOTYLEDONS  235 

VII.  FARIXALES.* — The  eleven  families  of  this  alliance  are 
Flagellariaceae,  Restionaceae,  Centrolepidaceae,  Mayacaceae, 
Xyridaceae,  Eriocaulaceae,  Rapateaceae,  Bromeliaceae,  Com- 
melinaceae,  Pontederiaceae,  and  Philydraceae,  together  contain- 
ing a  little  more  than  2,000  species.  The  large  families  are 
Bronieliaceae  with  over  900  species,  Eriocaulaceae  with  460, 
Cominelinaceae  with  more  than  300,  and  Restionaceae  with 
nearly  250.  The  chief  character  that  holds  these  diverse  fami- 
lies together  and  separates  them  from  the  Liliales  is  the  thin- 
walled  endosperm  rich  in  starch,  whose  cells  become  easily 
broken  up  and  dissociated,  resulting  in  a  "  mealy  "  or  "  crum- 
bly "  endosperm. 

From  the  evolutionary  standpoint  the  following  facts  are  of 
importance:  for  the  most  part  the  forms  are  grass-like  herbs, 
with  all  habits  from  aquatic  to  xerophytic  and  epiphytic ;  they 
are  mostly  bracteate  forms,  the  upper  bracts  showing  a  decided 
tendency  to  ensheath  the  inflorescence;  they  are  mostly  ane- 
mophilous,  but  some  forms  have  a  perianth  adapted  to  ento- 
mophily;  the  perianth  ranges  from  scarious  to  jTetaloid,  from 
undifferentiated  to  a  distinct  calyx  and  corolla,  from  polypetaly 
to  sympetaly ;  the  flowers  are  syncarpous  and,  with  the  excep- 
tion of  a  few  Brornelias,  hypogynous. 

Such  evidence  indicates  a  relatively  primitive  cyclic  alli- 
ance with  many  characters  recalling  the  spiral  forms,  the 
bract-protection  and  anemophily  not  being  definitely  replaced 
by  a  highly  developed  perianth  and  entomophily.  The  origin 
of  the  series  is  of  course  obscure,  but  the  evidence  seems  to 
favor  the  Glumales  as  the  original  stock.  As  illustrating  the 
construction  of  a  natural  sequence  of  families,  those  of  this 
alliance  may  be  used  as  follows : 

The  Flagellariaceae,  Restionaceae,  and  Centrolepidaceae, 
belonging  to  the  oriental  tropics  chiefly  of  the  Southern  Hemi- 
sphere, have  a  bracteate  undifferentiated  perianth  and  are  ane- 
mophilous,  in  habit  and  general  character  resembling  the  Spiral 
series. 

The  Mayacaceae,  Xyridaceae,  and  Eriocaulaceae  have  a  dif- 
ferentiated calyx  and  corolla,  and  orthotropus  ovules  with  very 
small  embryos.  These  three  families,  together  with  Restiona- 

*  FARIXOSAE  of  Engler. 


236  MORPHOLOGY  OF  ANGIOSPERMS 

ceae  and  Centrolepidaceae,  constitute  the  main  part  of  the  old 
group  Enantioblastae,  characterized  by  the  orthotropous  ovules. 

The  Rapateaceae,  chiefly  South  American,  have  a  distinct 
calyx  and  corolla,  anatropous  ovules,  and  small  embryos. 

The  Bromeliaceae,  the  great  epiphytic  family  of  the  Ameri- 
can tropics,  have  a  distinct  calyx  and  corolla,  anatropous  ovules, 
and  larger  elongated  embryos. 

The  Commelinaceae,  in  addition  to  the  distinct  calyx  and 
corolla,  show  a  tendency  to  zygomorphy.  This  family  has  the 
orthotropous  ovules  and  small  embryos  of  the  Enantioblastae, 
but  the  characters  given,  as  well  as  the  habit  and  inflorescence, 
seem  to  forbid  that  alliance. 

The  Pontederiaceae  and  the  Australasian  Philydraceae 
have  long  cylindrical  embryos,  a  general  tendency  to  a  reduced 
number  of  stamens  and  carpels,  and  in  the  latter  family  sym- 
petaly. 

VIII.  LILIALES.* — The  nine  families  of  this  alliance  are 
Juncaceae,  Stemonaceae,  Liliaceae,  Haemodoraceae,  Amarylli- 
daceae,  Velloziaceae,  Taccaceae,  Dioscoreaceae,  and  Iridaceae, 
together  comprising  almost  5,000  species.  The  largest  families 
are  Liliaceae  with  nearly  2,500  species,  Iridaceae  with  more 
than  1,000,  and  Amaryllidaceae  with  nearly  900. 

This  great  alliance  may  be  regarded  as  containing  the  typ- 
ical highly  developed  Monocotyledons.  It  is  characterized  by 
a  conspicuous  development  of  the  perianth  and  a  prevailing 
entomophilous  habit.  The  endosperm  cells  are  thick-walled  and 
in  general  contain  oil  rather  than  starch,  resulting  in  an  endo- 
sperm that  is  not  "  mealy,"  as  in  the  Farinales.  The  Junca- 
ceae, Haemodoraceae,  and  Velloziaceae  are  exceptions  in  pro- 
ducing a  starch-containing  endosperm,  but  the  cells  do  not  be- 
come dissociated.  In  passing  from  the  lower  members  of  the 
series  to  the  higher  there  is  a  transition  from  an  undifferenti- 
ated  scarious  perianth  to  a  differentiated  and  petaloideous  one ; 
and  from  hypogyny  to  epigyny,  the  four  lower  families  being 
hypogynous  and  the  five  higher  epigynous. 

The  sequence  of  families  begins  with  the  Juncaceae,  which 
with  their  grass-like  habit,  scarious  perianth,  and  starchy  en- 
dosperm, may  be  fairly  regarded  as  intermediate  between  Fari- 

*  LILIIFLORAE  of  Engler. 


CLASSIFICATION  OF   MONOCOTYLEDONS  237 

nales  and  Liliales.  The  Liliales  are  midway  in  the  series,  hav- 
ing attained  a  petaloideous  perianth  and  entoraophily,  and 
having  become  so  diversified  in  structure  and  habit  as  to  raise 
a  question  as  to  their  monophyletic  origin.  The  Arnaryllida- 
ceae  introduce  epigyny,  and  the  highly  specialized  Iridaceae 
complete  the  series.  The  last  six  families  are  in  great  need  of 
morphological  investigation  in  the  tropics  where  they  are  chiefly 
massed. 

The  genetic  connection  between  Liliales  and  Farinales 
seems  clear,  so  that  if  the  latter  are  regarded  as  derived  from 
the  Glumales,  the  former  must  be  referred  to  the  same  stock, 
probably  dissociating  early  from  the  Farinales. 

The  two  remaining  alliances  are  characterized  by  epigyny 
and  zygomorphy,  highly  specialized  entomophilous  structures, 
reduction  and  modification  of  stamens,  and  very  small  and  un- 
differentiated  embryos.  In  all  probability  they  are  not  genet- 
ically related,  but  they  resemble  one  another  more  than  they  do 
the  other  alliances. 

IX.  SCITAMIXALES.* — The  four  families  of  this  alliance 
are  Musaceae,  Zingiberaceae,  Cannaceae,  and  Marantaceae,  to- 
gether comprising  nearly  800  species,  500  belonging  to  the 
Zingiberaceae.  The  four  families  are  undoubtedly  genetically 
related,  although  the  first  two  are  restricted  to  the  oriental 
tropics,  and  the  last  two  to  the  occidental.  In  addition  to  the 
characters  mentioned  above,  the  replacing  of  functional  sta- 
mens by  petaloid  staminodia  is  very  characteristic,  commonly 
only  one  stamen  being  functional  and  even  this  one  being  peta- 
loid. In  nearly  every  case,  also,  there  is  a  labelluni,  formed 
either  by  the  perianth  or  the  staminodia.  The  habit  of  the  vege- 
tative body,  however,  is  most  peculiar.  The  real  stem  is  a  rhi- 
zome, but  the  enormous  leaves,  differentiated  into  sheath,  peti- 
ole, and  pinnately  veined  blade,  build  up  a  false  stem  by  means 
of  their  very  large  and  closely  overlapping  sheaths. 

The  temptation  is  to  derive  this  alliance  from  the  Dracaena 
region  of  the  Liliaceae,  but  important  anatomical  features  that 
are  common  to  all  four  families  are  opposed  to  this  view.  That 
it  i.s  connected  in  some  way  with  the  Glumales-Farinales-Lili- 
ales  stock  seems  most  probable ;  and  if  so  the  general  structures 

*  SCITAMINEAE  of  Engler. 


238  MORPHOLOGY  OF  ANGIOSPERMS 

indicate  a  separate  origin  from  Glumales.  A  morphological 
investigation  of  these  families  in  the  tropics  is  greatly  to  be 
desired. 

X.  OKCHIDALES.* — The  two  families  of  this  alliance  are 
Bnrmanniaceae  and  Orchidaceae,  all  but  about  55  of  the  7,000 
species  belonging  to  the  latter  family.  These  two  unequal  fami- 
lies are  held  together  by  the  very  numerous  and  small  ovules 
and  by  the  extreme  zygomorphism  of  the  flower,  but  the  Bur- 
manniaceae  have  endosperm,  often  six  stamens,  and  frequently 
connate  perianth-segments,  approaching  the  Amaryllidaceae. 

The  chief  interest  of  the  alliance  centers  about  the  Orchi- 
daceae>  the  greatest  monocotyledonous  family  in  point  of  spe- 
cies and  the  most  highly  specialized.  The  epiphytic  habit  is 
extensively  developed,,  and  the  terrestrial  forms  are  mostly 
saprophytic  or  parasitic.  These  habits  have  resulted  in  the 
development  of  certain  special  structures,  such  as  the  bulbous 
leaf-bases  and  velamen  of  the  epiphytic  forms ;  and  in  the  sup- 
pression of  some  normal  structures,  as  the  primary  root,  and 
sometimes  all  roots.  The  absence  of  endosperm,  the  poorly 
developed  embryo,  and  the  extensive  use  of  the  suspensor  as  a 
remarkably  developed  haustorial  organ  are  probably  but  addi- 
tional results  of  the  unusual  habits  of  the  family.  The  notable 
floral  structures  are  the  modification  of  one  of  the  petals  to 
form  the  labellum  and  spur,  the  remarkable  "  gynostemium," 
the  twisted  ovary,  and  the  pollinium-mechanism. 

As  an  illustration  of  the  varying  modifications  of  floral 
structure,  the  ordinary  orchid  may  be  compared  with  the  Cy- 
pripedium  type.  The  flowers  are  pentacyclic,  and  the  cycles 
are  developed  in  the  two  types  as  follows,  beginning  with  the 
outermost.  In  both  types  the  first  cycle  consists  of  three  sepals, 
and  the  second  of  three  petals,  the  posterior  (made  anterior  by 
the  twisting  of  the  ovary)  forming  the  labellum  and  spur.  In 
the  third  cycle  two  lateral  stamens  are  suppressed  in  both  types, 
but  in  ordinary  orchids  the  anterior  one  is  functional,  while 
in  Cypripedium  it  is  replaced  by  a  staminodium.  In  the  fourth 
cycle  the  posterior  stamen  is  suppressed  in  both  types,  but  in 
ordinary  orchids  the  two  laterals  are  replaced  by  staminodia, 
while  in  Cypripedium  they  are  functional  stamens.  In  the 

*  MICROSPERMAE  of  Engler. 


CLASSIFICATION  OF  MONOCOTYLEDONS  239 

fifth  cycle  in  ordinary  orchids  the  two  lateral  carpels  form  the 
stigma,  the  anterior  producing  the  disk-bearing  "  rostellum," 
while  in  Cypripedium  all  three  carpels  form  the  stigma. 

The  origin  of  the  Orchidaceae  is  very  obscure.  It  is  com- 
mon to  regard  them  as  derived  from  the  Liliales,  but  there  are 
many  objections  to  this  hypothesis.  In  any  event,  it  seems 
most  natural  to  refer  them  to  the  same  general  stock. 

According  to  the  views  presented  in  this  chapter,  there  are 
three  primitive  monocotyledonous  stocks — Pandanales.  Helobi- 
ales,  and  Glumales — and  they  are  connected  with  the  other 
alliances  as  follows:  Pandanales-Palmales-Synanthales;  Helo- 
biales-Arales ;  Glumales-Farinales-Liliales-Scitaminales-Orchi- 
dales. 


CHAPTEE    XI 

CLASSIFICATION    OF   ARCHICHLAMYDEAE 

Two  great  divisions  of  Dicotyledons  are  evident,  the  Archi- 
chlamydeae  and  Sympetalae,  although  there  is  no  sharp  distinc- 
tion between  them.  Sympetalous  forms  among  the  former  and 
polypetalous  forms  among  the  latter  occur,  but  in  the  main 
apetaly  or  polypetaly  is  a  distinctive  feature  of  the  Archichla- 
mydeae,  and  sympetaly  of  the  Sympetalae.  That  the  Archi- 
chlamydeae  include  the  most  primitive  Dicotyledons  is  clear, 
but  what  forms  are  to  be  regarded  as  the  most  primitive  is  open 
to  discussion. 

The  classification  of  the  Archichlamydeae  is  an  exceedingly 
puzzling  problem,  and  the  current  schemes  are  far  less  definite 
and  satisfactory  than  those  for  the  classification  of  Monocotyle- 
dons and  Sympetalae.  Questions  of  primitive  and  reduced 
characters,  and  of  relative  rank  on  the  basis  of  combination  of 
characters,  are  particularly  involved  among  Archichlamydeae, 
and  hence  opinions  vary  widely  as  to  the  details  of  their  classi- 
fication. The  difficulties  arise  from  the  fact  that  the  characters 
of  the  group  are  extremely  fluctuating,  not  being  established 
as  among  the  Sympetalae.  Add  to  this  that  more  than  60,000 
species  *  are  recognized,  over  three  times  as  numerous  as  the 
species  of  Monocotyledons,  included  in  180  families,  and  it 
becomes  evident  that  the  confusion  of  relationships  is  bewil- 
dering. 

Engler  has  arranged  the  Archichlamydeae  in  twenty-six  al- 

*  The  numbers  of  species  given  in  this  chapter  must  be  regarded  as  approx- 
imate and  conservative.     They  will  vary  with  the  increase  of  knowledge  and 
the  conception  of  species,  but  in  this  chapter  they  are  only  intended  to  indi- 
cate the  relative  display  of  different  types  of  structure. 
240 


CLASSIFICATION   OF  ARCHICHLAMYDEAE 

liances,  coordinate  with  the  ten  series  of  Monocotyledons.  The 
general  sequence  of  these  alliances  is  based,  as  in  Monocotyle- 
dons, upon  the  development  of  the  perianth  and  of  the  floral  axis, 
and  the  arrangement  of  floral  members;  but  other  characters, 
chiefly  those  derived  from  the  ovules,  are  also  used  to  disen- 
tangle relationships.  Of  course  there  is  no  real  sequence  of 
these  twenty-six  alliances,  for  they  represent,  for  the  most  part, 
parallel  or  divergent  lines  of  development.  The  sequence  of 
presentation  is  determined  in  the  main  by  the  relative  advance- 
ment of  the  lower  members  of  each  alliance,  whose  higher  mem- 
bers may  or  may  not  have  made  great  advancement  and  in  many 
directions.  Such  an  assemblage  of  forms  may  be  conceived  of  as 
a  tangled  thicket,  through  which  certain  paths  may  be  more  or 
less  evident,  but  in  which  no  orderly  arrangement  is  apparent. 
It  would  be  confusing,  even  were  it  possible,  to  discuss  the 
relationships  of  each  of  the  twenty-six  series.  They  can  only 
be  presented  as  assemblages  of  families  that  seem  to  be  natural, 
perhaps  not  so  much  on  account  of  their  common  origin  as  on 
account  of  their  approximately  equal  grade  of  advancement, 
and  hence  "  form-groups "  rather  than  necessarily  genetic 
groups. 

The  following  presentation  of  the  alliances  of  Archichlamy- 
deae  is  largely  based  upon  Engler's  "  Uebersicht  iiber  die  Unter- 
abteilungen,  Klassen,  Reihen,  Unterreihen,  und  Familien  der 
Embryophyta  siphonogama,"  published  in  Engler  and  Prantl's 
Die  Naturlichen  Pflanzenfamilien  in  1897  (Lieferung  165). 

The  first  twelve  alliances  are  especially  puzzling.  Among 
them  are  evidently  the  most  primitive  forms  in  floral  structure. 
They  also  include  the  chalazogamic  forms,  and  ovules  whose 
structure  is  unusual  among  Angiosperms.  The  families  are 
practically  those  that  were  disposed  of  by  Eichler  as  Amen- 
tiferae,  together  with  miscellaneous  groups  of  uncertain  affinity. 
That  the  so-called  Amentiferae  or  Amentaceae  represented  a 
heterogeneous  assemblage  of  forms  has  long  been  evident.  It  is 
a  question  whether  Engler's  splitting  up  into  alliances  has  not 
been  excessive  in  this  part  of  his  scheme,  certain  morphological 
characters  sometimes  being  used  that  may  not  prove  to  be  of 
first  importance.  In  any  event,  the  splitting  up  will  serve  to 
keep  apart  distinct  groups  until  they  can  be  recombined  natu- 
rally. There  is  no  region  of  the  Archichlamydeae  which  has 


242  MORPHOLOGY  OF  ANGIOSPERMS 

recently  received  more  deserved  attention  from  morphologists, 
and  which  still  so  greatly  needs  investigation. 

I.  CASUARINALES.* — This  includes  the  single  family  Casu- 
arinaceae,  containing  about  25  species.     Engier  regards  the  al- 
liance as  the  most  primitive  because  the  ovule  develops  numer- 
ous megaspores.     This  particular  character  can  not  be  regarded 
as  distinctive,   since  among  the  Fagales  the  same  character, 
associated  also  with  chalazogamy,  occurs,  and  numerous  mega- 
spores  are  found  among  the  Ranales,  Resales,  etc.     The  low 
position,  however,  is  justified  by  the  primitive  flowers,  which 
are  either  naked  or  with  a  bract-like  perianth. 

The  next  two  alliances  are  regarded  as  relatively  primitive 
on  account  of  their  naked  flowers,  together  with  the  Casuari- 
nales  being  the  only  naked  alliances. 

II.  PIPERALES. — This   includes   the   Saururaceae,    Pipera- 
ceae,  Chloranthaceae,  and  Lacistemaceae,  together  containing 
about  1,150  species,  of  which  about  1,100  belong  to  the  Pipera- 
ceae.     The  results  of  the  investigation  of  Peperomia  pcllucida 
by  Campbell  and  by  Johnson  indicate  that  the  tropical  Pipera- 
ceae   are   probably   most   promising   forms   for   morphological 
investigation,  and  are  to  be  considered  in  any  discussion  as  to 
the  most  primitive  Dicotyledons. 

III.  SAI/TCALES. — This  includes  the  single  family   Salica- 
ceae,  containing  about  180  species. 

IV.  MYRICALES. — This  includes  the  single  family  Myrica- 
ceae,  containing  40  species.     The  advance  in  floral  structure  is 
shown  by  the  fact  that  the  several  bracts  near  the  flower  may 
be  regarded  as  an  extremely  primitive  perianth. 

V.  BALANOPSIDALES. — This  includes  the  single  family  Ba- 
lanopsidaceae,  containing  7  species.     This  is  an  uncertain  type, 
and  raises  the  question  of  reduction.      The  staminate  flowers 
have  a  rudimentary  perianth  and  an  indefinite  number  of  sta- 
mens;  and  the  carpellate  flowers  have   a   bracteate   perianth. 
Engier  calls  attention,  however,  to  the  fact  that  there  are  no 
intermediate  forms  for  a  reduction  series,  and  that  the  indefi- 
nite number  of  stamens  is  a  primitive  character. 

VI.  LEITNERIALES. — This  includes  the  single  family  Leit- 
neriaceae,  containing  2  species.     The  primitive  character  of  this 

*  VERTICILLATAE  of  Engier. 


CLASSIFICATION  OF  ARCHICHLAMYDEAE  243 

type,  with  its  flowers  naked  or  with  a  bracteate  perianth,  is 
very  doubtful.  Engler  states  that  if  any  evidence  of  reduction 
is  obtained,  this  family  would  be  included  among  the  Rosales, 
near  the  Haniamelidaceae. 

VII.  JUGLAXDALES. — This  includes  the  single  family  Ju- 
glandaceae,  containing  about  30  species.     This  alliance  is  dis- 
tinctly higher  than  the  preceding  ones  in  that  there  is  nearly 
always  a  distinct  perianth,  which  in  the  carpellate  flowers  is 
coalescent  with  the  ovary,  so  that  there  is  a  resemblance  to 
epigyny.     Disregarding  the  Balanopsidales  and  Leitneriales  as 
doubtful  and  possibly  reduction  alliances,  the  Juglandales  are  to 
be  compared  directly  with  the  Myricales.     The  two  were  for- 
merly associated  in  a  single  alliance,  but  the  distinct  perianth, 
as  well  as  chalazogamy,  serve  to  distinguish  the  Juglandales. 
It  is  a  question  whether  such  differences,  and  the  others  asso- 
ciated with  them,  are  incompatible  in  a  single  alliance. 

VIII.  FAGALES. — This  includes  the  Betulaceae  and  Faga- 
ceae,  together  containing  about  420  species,  nearly  350  of  which 
belong  to  the  Fagaceae.    This  is  a  parallel  alliance  with  Juglan- 
dales, having  a  distinct  but  bracteate  perianth,  which  in  the 
carpellate  flowers  is  more  or  less  coalescent  with  the  ovary. 
Among  Betulaceae,  also,  chalazogamy  occurs,  as  in  Juglanda- 
ceae  and  Casuarinaceae. 

IX.  URTICALES. — This  includes  the  Ulmaceae,  Moraceae, 
and  Urticaceae,  together  containing  about  1,560  species,  the 
large  families  being  Moraceae  with  about  920  species,  and  the 
Urticaceae  with  about  520.     This  is  an  alliance  parallel  with 
the  Juglandales  and  Fagales,  with  the  distinct  and  bracteate 
perianth,  which,  as  in  Fagales,  is  definitely  cyclic. 

X.  PROTEALES. — This  includes  the  single  great  Australasian 
family  Proteaceae,  with  about  950  species.     In  this  alliance 
the  next  stage  in  the  development  of  the  cyclic  perianth  becomes 
evident.     Although  it  is  sometimes  green  and  bract-like,  in  the 
majority  of  cases  it  is  petaloid,  but  there  is  no  differentiation  of 
calyx  and  corolla.     A  character  used  to  distinguish  this  alliance 
from  the  following  is  the   single  carpel  with  well-developed 
ovule. 

XI.  SAXTALALES. — This  includes  the  Loranthaceae,  Myzo- 
dendraceae,    Santalaceae,   Grubbiaceae,   Opiliaceae,    Olacaceae, 
and  Balanophoraceae,  together  containing  about  1,260  species, 


244  MORPHOLOGY  OF  ANGIOSPERMS 

the  large  families  being  Loranthaceae  with  800  species,  Santa- 
laceae  with  246,  and  Olacaceae  with  150.  In  this  alliance,  also, 
the  cyclic  perianth  is  for  the  most  part  petaloid,  but  there  is 
advancement  in  the  general  differentiation  of  a  calyx  and  co- 
rolla. For  the  most  part,  there  is  a  syncarpous  pistil  of  three 
carpels,  but  the  carpels  may  be  two  or  one;  and  a  free  central 
placenta  develops  ovules  without  an  integument  or  no  distinct 
ovules  at  all.  There  is  much  diversity  within  the  alliance,  at 
least  three  distinct  lines  being  evident;  but  the  rather  remark- 
able morphological  structures  found  in  the  alliance  are  prob- 
ably related  to  their  general  parasitic  or  semi-parasitic  habits. 

XII.  ARISTOLOCHIALES. — This    includes   the   Aristolochia- 
ceae,  Kafflesiaceae,  and  Hydnoraceae,  together  containing  about 
235  species,  of  which  205  belong  to  the  Aristolochiaceae.     The 
members  of  this  series  are  distinctly  in  advance  of  the  preceding 
in  the  coalescence  of  the  petaloid  segments  of  the  perianth,  and 
especially  in  epigyny.     The  indefinite  number  of  ovules  is  also 
a  distinguishing  feature. 

The  preceding  twelve  alliances  represent  a  primitive  com- 
plex, in  which  reduced  forms  may  have  been  included.  How 
they  may  be  related  to  one  another  in  origin  is  too  obscure  for 
profitable  discussion,  but  it  seems  probable  that  they  are  not  at 
all  related  to  the  following  alliances.  In  other  wrords,  whether 
they  represent  a  single  genetic  stock  or  several,  they  appear  to 
be  isolated  from  the  higher  alliances. 

XIII.  POLYGONALES. — This    includes    the    single    family 
Polygonaceae,    with    about    750    species.      Its    mostly    cyclic 
flowers,  with  undifferentiated  perianth  or  distinct  calyx  and 
corolla,  puts  it  upon  about  the  plane  of  advancement  attained 
by  the  preceding  alliances ;  while  its  strong  trimerous  tendency 
and  peculiar  habit  set  it  well  apart.      This  is  sometimes  re- 
garded as  a  transition  group  between  the  preceding  alliances 
and  the  Centrospermales.     In  any  event,  it  may  be  regarded 
as  fairly  associated  with  the  latter. 

XIV.  CENTROSPEE^IALES.*     -  This    includes    Chenopodia- 
ceae,  Amarantaceae,  Xyctaginaceae,  Batidaceae,  Cynocramba- 
ceae,  Phytolaccaceae,  Aizoaceae,  Portulacaceae,  Basellaceae,  and 
Caryophyllaceae,  together  containing  about  3,320  species,  the 

*  CENTROSPERMAE  of  Engler. 


CLASSIFICATION  OF  ARCHICHLAMYDEAE  245 

large  families  being  Caryophyllaceae  with  1,420  species,  Aizoa- 
ceae  with  575,  and  Chenopodiaceae  and  Amarantaceae  each 
with  about  435.  In  this  alliance  the  floral  characters  range 
from  the  bracteate  undiiferentiated  perianth  of  Chenopodiaceae 
to  the  distinct  calyx  and  corolla  of  many  Caryophyllaceae.  In 
the  alliance  as  a  whole  calyx  and  corolla  are  frequently  rather 
than  prevailingly  distinct,  and  only  the  highest  family  has  at- 
tained the  conspicuous  corolla  associated  with  entomophily.  A 
feature  of  the  alliance  is  the  conspicuous  perisperm. 

The  Polygonales  and  Centrospermales  may  possibly  have  a 
closely  related  origin,  but  it  does  not  seem  probable  that  they 
are  related  in  any  way  to  the  following  alliance,  but  that  they 
represent  a  general  line  of  development  whose  highest  expres- 
sion is  among  the  Caryophyllaceae. 

XV.  EAXALES. — This  includes  Xyrnphaeaceae,  Ceratophyl- 
laceae,  Trochodendraceae,  Ranunculaceae,  Lardizabalaceae,  Ber- 
beridaceae,  Menispermaceae,Magnoliaceae,  Calycanthaceae,  Lac- 
toridaceae,  Anonaceae,  Myristicaceae,  Gomortegaceae,  Monimia- 
ceae,  Lauraceae,  and  Hernandiaceae,  together  containing  about 
4,050  species,  the  large  families  being  Lauraceae  with  1,015 
species,  Ranuncalaceae  with  990,  Menispermaceae  with  390, 
Anonaceae  with  345,  Monirniaceae  with  245,  Myristicaceae  with 
235,  and  Berberidaceae  with  135. 

This  great  alliance  introduces  the  prevailing  habit  of  a  dis- 
tinct calyx  and  corolla,  and  is  characterized  by  the  prevalence 
of  apocarpy  and  hypogyny.  The  primitive  character  of  the 
flower  is  indicated  not  only  by  apocarpy  and  hypogyny,  but  also 
by  the  strong  tendency  to  the  indefinite  repetition  and  spiral 
arrangement  of  the  floral  members.  Were  it  not  for  the  preva- 
lence of  a  distinct  calyx  and  corolla  the  alliance  would  not  hold 
so  high  a  rank.  At  least  three  prominent  developmental  lines 
are  evident,  viz.,  Xymphaeaceae  to  Ceratophyllaceae,  Ranun- 
culaceae  to  Menispermaceae,  and  Magnoliaceae  to  Hernandia- 
ceae. In  each  of  these  lines  there  is  an  advance  from  the 
spiral  to  the  cyclic  arrangement,  and  in  the  last  line  epigyny 
is  reached.  As  is  also  known,  zygomorphy  occasionally  occurs, 
being  present  in  no  preceding-  alliance  except  the  Aristolochiales. 

It  seems  probable  that  the  higher  alliances  of  the  Archichla- 
mydeae  are  related  in  some  way  to  the  Ranales,  whose  numerous 
lines  of  development  seem  to  have  been  taken  up  by  other 


246  MORPHOLOGY  OF  ANGIOSPERMS 

alliances.  It  follows  that  the  subsequent  alliances  will  touch  the 
Ranales  in  various  ways,  the  latter  representing  a  plexus  out  of 
which  various  divergent  lines  have  become  distinct.  This  con- 
ception of  the  genetic  position  of  Ranales  among  Archichlamy- 
deae  has  brought  to  them  the  attention  of  morphologists,  and 
the  results  thus  far  have  more  than  justified  their  investigation. 

XVI.  RHOEDALES. — This    includes    Papaveraceae,    Cruci- 
ferae, Tovariaceae,  Capparidaceae,  Resedaceae,  and  Moringa- 
ceae,  together  containing  about  2,615  species,  the  large  families 
being  Cruciferae  with  1,860  species,  Capparidaceae  with  425, 
and  Papaveraceae  with  280.     There  seems  to  be  no  question 
that  this  alliance  is  closely  related  to  the  Ranales.     The  connec- 
tion seems  to  be  through  the  Papaveraceae,  which  exhibit  struc- 
tures resembling  those  of  Xymphaeaceae ;  while  the  transition 
from  Papaveraceae  to  Cruciferae  through  the  Fumaria  forms 
is  plain,  and  the  affinity  of  Cruciferae  and  Capparidaceae  is 
unquestioned. 

XVII.  SAKRACENIALES.  —  This    includes     Sarraceniaceae, 
Nepenthaceae,  and  Droseraceae,  together  containing  145  spe- 
cies, nearly  100  of  which  belong  to  the  Droseraceae.      The 
alliance  is  evidently  parallel  with  Rhoedales,  and  both  are  cer- 
tainly related  to  the  ^Nymphaeaceae-region  of  the  Ranales.     In 
fact,  the  Xymphaeaceae,  Papaveraceae,  and  Sarraceniales  have 
many  things  in  common  in  the  arrangement  of  floral  members 
and  the  spirocyclic  character  of  the  flowers.     The  distinctive 
character  of  Sarraceniales  as  compared  with  Rhoedales  is  the 
prevalence  in  the  former  of  central  placentation. 

XVIII.  ROSALES.— This    includes    Podostemonaceae,    Hy- 
drostachyaceae,    Crassulaceae,    Cephalotaceae,     Saxifragaceae, 
Pittosporaceae,  Brunelliaceae,   Cunoniaceae,  Myrothamnaceae, 
Bruniaceae,  Hamamelidaceae,  Platanaceae,   Crossosomataceae, 
Rosaceae,  Connaraceae,  and  Leguminosae,  together  containing 
about  14,270  species,  the  large  families  being  Leguminosae  with 
over  11,000  species,  Rosaceae  with  1,525,  Saxifragaceae  with 
630,  and  Crassulaceae  with  490.     Since  this  alliance  contains 
by  far  the  greatest  family  of  Archichlamydeae,  in  fact,  with  a 
single  exception,  the  greatest  family  of  Angiosperms,  it  may 
be  regarded  as  the  most  representative  and  dominant  alliance. 

The  beginnings  of  this  great  alliance,  with  apocarpy,  hypo- 
gyny,  and  indefinite  repetition  of  certain  floral  members,  have 


CLASSIFICATION  OF  ARCHICHLAMYDEAE  247 

much  in  common  with  the  Ranales,  especially  the  line  con- 
taining Ranunculaceae.  However,  it  has  reached  a  much  higher 
development  in  the  more  frequent  occurrence  of  syncarpy,  and 
also  of  perigyny  and  epigyny,  and  especially  in  the  remarkable 
development  of  zygomorphy  among  the  Leguminosae.  Disre- 
garding the  smaller  families,  the  Saxifragaceae  may  be  regard- 
ed as  the  beginnings  of  the  alliance,  originating  in  the  Ranales, 
and  diverging  toward  Podostemonaceae  in  one  direction  and 
Roeaceae-Leguminosae  in  the  other.  It  has  long  been  known 
that  there  is  no  real  distinctive  character  separating  Saxifraga- 
ceae and  Rosaceae ;  and  the  transition  from  the  latter  family  to 
the  Leguminosae  is  easy.  Rosaceae  are  characterized  by  actino- 
morphic  flowers  and  several  carpels;  while  Leguminosae  have 
zygomorphic  floAvers  and  a  single  carpel ;  but  there  are  members 
of  the  two  families  that  exactly  reverse  these  distinctions.  There 
seems  to  be  a  general  plexus  formed  by  the  Rosa  tribe  of  Rosa- 
ceae and  the  Mimosa  tribe  of  Leguminosae,  which  is  not  very 
far  removed  from  the  Ranunculaceae  among  Ranales.  Out  of 
the  Eosa  tribe  the  two  very  distinct  lines  of  drupe-forms  and 
pome-forms  have  diverged ;  while  the  Mimosa  tribe,  with  its 
actinomorphic  flowers  and  numerous  usually  free  stamens,  leads 
through  the  Caesalpinia  tribe,  with -its  actinomorphic  or  zygo- 
morphic flowers  and  free  stamens,  to  the  Papilio  tribe  with  its 
strongly  zygomorphic  flowers  and  coalescent  stamens. 

The  culmination  of  the  alliance  is  of  course  the  elaboration 
of  zygomorphy,  the  Leguminosae  dominating  in  this  regard 
among  Archichlamydeae,  as  do  the  Orchidaceae  among  Monoco- 
tyledons, and  the  Personales  among  Sympetalae. 

In  the  preceding  related  alliances,  from  Ranales  to  Rosales, 
the  cyclic  character  of  the  flower  is  not  fully  established,  every 
line  of  development  having  spiral  members.  In  the  following 
alliances,  however,  the  cyclic  character  is  fully  established. 

XIX.  GERAXIALES. — This  includes  Geraniaceae,  Oxalida- 
ceae,  Tropaeolaceae,  Linaceae,  Humiriaceae,  Erythroxylaceae, 
Zygophyllaceae,  Cceoraceae,  Rutaceae,  Simarubaceae,  Bursera- 
ceae,  Meliaceae,  Malpighiaceae,  Trigoniaceae,  Vochysiaceae, 
Tremandraceae,  Polygalaceae,  Dichapetalaceae,  Euphorbiaceae, 
and  Callitrichaceae,  together  containing  about  9,160  species, 
the  large  families  being  Euphorbiaceae  with  4,140  species,  Ru- 
taceae  with  910,  Meliaceae  with  753,  Malpighiaceae  with  700, 

IT 


248  MORPHOLOGY  OF  ANGIOSPERMS 

Polygalaceae  with  667,  Geraniaceae  with  455,  Oxalidaceae  with 
330,  and  Burseraceae  with  320. 

This  cyclic  alliance  begins  with  those  families  that  are  iso- 
carpic  and  extends  to  those  in  which  a  reduction  in  the  number 
of  carpels  is  prevalent.  It  is  chiefly  distinguished  from  the 
Sapindales,  with  which  it  is  parallel  and  very  closely  allied, 
by  the  orientation  of  the  ovules,  the  raphe  of  the  anatropous 
ovules  being  ventral  in  Geraniales  and  dorsal  in  Sapindales. 
Just  the  significance  of  such  a  character  in  distinguishing  great 
genetic  alliances  is  not  clear,  but  its  constancy  is  in  its  favor. 
Three  lines  of  development  are  evident,  the  most  prominent 
beginning  with  Geraniaceae,  including  the  zygomorphic  and 
anisocarpic  Tropaeolaceae  and  the  completely  syncarpic  Lina- 
ceae  and  its  allies,  and  ending  in  Cneoraceae  to  Meliaceae  with 
oil-cells  and  highly  differentiated  tissues.  Another  line  is  Mal- 
pighiaceae  to  Vochysiaceae,  characterized  by  oblique  zygomor- 
phy;  while  Polygalaceae  with  its  strongly  zygomorphic  flowers, 
Dichapetalaceae,  and  Euphorbiaceae,  show  no  surviving  fea- 
tures in  common.  The  affinities  of  these  last  three  families 
are  extremely  doubtful,  and  those  of  Callitrichaceae  are  even 
more  so. 

XX.  SAPINDALES.* — This  includes  Buxaceae,  Empetra- 
ceae,  Coriariaceae,  Limnanthaceae,  Anacardiaceae,  Cyrillaceae, 
Pentaphylaceae,  Corynocarpaceae,  Aquifoliaceae,  Celastraceae, 
Hippocrateaceae,  Stackhousiaceae,  Staphyleaceae,  Icacinaceae, 
Aceraceae,  Hippocastanaceae,  Sapindaceae,  Sabiaceae,  Meli- 
anthaceae,  and  Balsaminaceae,  together  comprising  about  3,125 
species,  the  large  families  being  Sapindaceae  with  1,040  species, 
Celastraceae  with  425,  Anacardiaceae  with  395,  Balsaminaceae 
with  300,  and  Aquifoliaceae  with  285. 

As  among  Geraniales,  the  alliance  begins  with  isocarpic 
forms  and  passes  to  those  in  which  the  number  of  carpels  is 
reduced,  and  in  the  higher  families  zygomorphy  is  attained. 
The  orientation  of  the  ovules  that  separates  this  alliance  from 
the  Geraniales  was  referred  to  under  that  alliance.  Engler  rec- 
ognizes so  many  lines  of  development  among  Sapindales  that 
the  alliance  seems  to  be  well  broken  up,  and  the  different  mem- 
bers not  clearly  related  to  one  another. 

*  Sometimes  called  CELASTRALES. 


CLASSIFICATION  OF  ARCHICHLAMYDEAE  249' 

XXI.  RHAMXALES. — This  includes  Rhamnaceae  and  Vita- 
ceae,   together   containing   about   955    species,    almost   exactly 
equally  distributed  between  the  two  families.     The  alliance  is 
clearly  parallel  with  the  preceding  one,  but  is  distinctly  set 
apart  by  its  tetracyclic  flowers  with  opposite  stamens. 

XXII.  MALVALES. — This  includes  Elaeocarpaceae,  Chlae- 
naceae,  Gonystylaceae,  Tiliaceae,  Malvaceae,  Triplochitonaceae, 
Bombacaceae,  Sterculiaceae,  and  Scytopetalaceae,  together  con- 
taining about  1,740  species,  the  large  families  being  Malvaceae 
with   about   800   species,   and   Sterculiaceae  with   780.      This 
alliance  is  very  uneven  in  the  advancement  of  its  characters,  and 
in  certain  features  would  seem  to  precede  Geraniales  and  Sa- 
pindales  in  any  sequence;  but  it  is  so  closely  related  to  Parie- 
tales  through  Elaeocarpaceae  and  Chlaenaceae  that  it  seems 
clear  it  should  be  placed  near  them. 

Distinct  or  slightly  united  carpels  are  found,  as  among  the 
Geraniales  and  Sapindales,  but  complete  syncarpy  prevails. 
The  inequality  of  advancement  is  shown  in  such  families  as 
Tiliaceae,  in  which  there  is  complete  syncarpy  associated  with 
indefinite  stamens;  and  Sterculiaceae,  in  which  there  is  a  com- 
plexity in  the  arrangement  of  stamens  approaching  that  in 
Malvaceae,  associated  with  a  more  or  less  incomplete  union  of 
carpels. 

XXIII.  PARIETALES. — This     includes     Dilleniaceae,     Eu- 
cryphiaceae,  Ochnaceae,  Caryocaraceae,  Marcgraviaceae,  Qui- 
inaceae,  Theaceae,  Guttiferae,  Dipterocarpaceae,  Elatinaceae, 
Frankeniaceae,  Tamaricaceae,  Fouquieraceae,  Cistaceae,  Bixa- 
ceae,   Cochlospermaceae,   Koeberliniaceae,    Canellaceae,   Yiola- 
ceae,  Flacourtiaceae,  Stachyuraceae,  Turneraceae,  Malesherbia- 
ceae,  Passifloraceae,  Achariaceae,  Caricaceae,  Loasaceae,  Datis- 
caceae,  Begoniaceae,  and  Ancistrocladaceae,  together  compris- 
ing about  4,225   species,  the  large  families  being  Guttiferae 
with  760  species,  Flacourtiaceae  with  525,  Begoniaceae  with 
405,  Yiolaceae  with  400,  Dipterocarpaceae  with  320,  and  Pas- 
sifloraceae with  315. 

The  Parietales  are  prevailingly  syncarpous,  and  have  very 
evident  connection  with  the  Ranales  through  the  Dilleniaceae, 
which  were  formerly  included  among  the  Ranales,  and  with 
the  Rhoedales  through  the  Flacourtiaceae  and  other  families. 
The  families  from  Dilleniaceae  to  Dipterocarpaceae,  mainly 


250  MORPHOLOGY  OF  ANGIOSPERMS 

tropical,  are  regarded  as  one  line,  characterized  by  an  oily  en- 
dosperm; and  among  them  such  primitive  characters  as  the 
spiral  arrangement  and  indefinite  number  of  floral  members 
occur,  and  even  apocarpy  (Ochnaceae).  Another  line  includes 
the  Elatinaceae  to  the  Frankeniaceae,  chiefly  a  temperate  group 
characterized  by  a  starchy  endosperm.  The  Fouquieraceae  are 
regarded  as  independent  of  the  last  line  on  account  of  their 
sympetaly  and  oily  endosperm.  The  Cistaceae  and  Bixaceae 
also  form  an  independent  line  with  starchy  endosperm.  The 
Cochlospermaceae  and  Koeberliniaceae  are  also  regarded  as 
independent  and  much  resemble  the  Capparidaceae  among  the 
Khoedales.  The  families  from  Canellaceae  to  Achariaceae  form 
another  line,  all  characterized  by  oily  endosperm,  starting  with 
completely  cyclic  flowers,  and  leading  to  such  special  develop- 
ments as  a  strong  tubular  development  of  the  receptacle  and 
even  sympetaly  (Achariaceae).  Closely  related  to  this  line  are 
the  Caricaceae,  with  sympetalous  corollas,  but  distinguished  by 
their  stamens  and  latex  system.  The  last  four  families  (Loasa- 
ceae  to  Ancistrocladaceae)  are  epigynous,  but  each  one  seems  to 
be  a  peculiar  and  isolated  type  of  development.  This  complex 
alliance  is  a  good  illustration  of  divergent  lines  of  development 
within  one  general  circle  of  affinity,  and  at  the  same  time  of  a 
gradual  increase  in  floral  complexity. 

XXIV.  OPUNTIALES. — This    includes    the    single    family 
Cactaceae,  with  about  1,000  species.     This  characteristic  Amer- 
ican family  presents  a  strange  mixture  of  primitive  and  ad- 
vanced characters  in  the  structure  of  the  flower.     The  spiral 
arrangement  and  indefinite   repetition  of  floral  members   are 
often  as  primitive  as  in  the  Nymphaeaceae,  with  which  region 
of  the  Ranales  the  alliance  may  be  connected.     The  tubular 
receptacle,  however,  enclosing  the  constantly  syncarpous  pistil 
relates  the  group  to  the  Parietales. 

XXV.  MYRTALES. — This  includes  the  Geissolomaceae,  Pe- 
naeaceae,    Oliniaceae,    Thymelaeaceae,    Elaeagnaceae,    Lythra- 
ceae,  Sonneratiaceae  (Blattiaceae),  Punicaceae,  Lecythidaceae, 
Rhizophoraceae,    Combretaceae,    Myrtaceae,    Melastomataceae, 
Onagraceae,  Hydrocaryaceae,    Haloraghidaceae,  and  Cynomo- 
riaceae,  together  containing  about  7,180  species,  the  large  fami- 
lies being  Melastomataceae  with  2,750  species,  Myrtaceae  with 
2,565,  Onagraceae  with  465,   Thymelaeaceae  with   395,   and 


CLASSIFICATION  OF   ARCHICHLAMYDEAE  251 

Lythraceae  with  340.  The  high  character  of  this  alliance  is  in- 
dicated by  the  constantly  perigynous  and  epigynous  flowers,  as 
well  as  by  the  constantly  cyclic  stamens,  and  the  tendency  to 
tetramerous  flowers  is  strong. 

XXVI.  UMBELLALES.* — This  includes  the  Araliaceae, 
Umbelliferae,  and  Cornaceae,  together  containing  about  2,660 
species,  about  2,100  of  which  belong  to  the  Umbelliferae.  The 
series  is  clearly  the  ranking  one  among  the  Archichlamydeae  on 
account  of  its  epigyny,  cyclic  stamens,  reduced  number  of  car- 
pels, and  mostly  reduced  sepals,  the  floral  formula  being  the 
same  as  that  of  the  highest  Sympetalae.  The  three  families 
constituting  the  alliance  are  very  closely  related,  and  the  alliance 
as  a  whole  stands  so  stiffly  apart  from  other  Archichlamydeae 
as  to  raise  the  question  whether  it  does  not  really  belong  among 
the  higher  Sympetalae. 

It  will  be  noted  that  in  a  large  sense,  and  with  the  excep- 
tion of  the  last  two  alliances,  the  Archichlamydeae  correspond 
to  the  Spiral  series  among  Monocotyledons,  in  which  the  cyclic 
arrangement,  although  it  frequently  appears,  is  not  fully  estab- 
lished in  every  set  of  floral  members.  In  the  same  sense,  there- 
fore, the  Myrtales,  Umbellales,  and  Sympetalae,  correspond  to 
the  Cyclic  series  among  Monocotyledons. 

*  UMBELLIFLORAE  of  Engler. 


CHAPTER    XII 

CLASSIFICATION   OF    SYMPETALAE 

THE  Sympetalae  form  a  much  better  defined  group  than  do 
the  Archichlamydeae,  from  which  they  seem  to  have  been  de- 
rived. The  sympetalous  character  is  almost  universal,  and 
justifies  the  name  of  the  group.  To  regard  it  as  the  crucial 
test,  however,  is  to  introduce  the  flavor  of  an  artificial  system. 
Among  the  Archichlamydeae  sympetalous  forms  were  noted, 
and  certain  families  of  the  Sympetalae  include  polypetalous 
members.  It  would  seem  that  such  exceptions  might  apply  to 
whole  families,  whose  other  characters  would  determine  their 
affinities.  For  example,  the  Umbelliferae  present  the  combina- 
tion of  characters  that  belongs  to  the  Sympetalae,  excepting 
sympetaly;  and  this  exception  does  not  seem  to  be  a  sufficient 
reason  to  exclude  them  from  association  among  the  epigynous 
anisocarpic  Sympetalae,  any  more  than  the  polypetaly  of  the 
Pirolaceae  excludes  them  from  the  isocarpic  Sympetalae. 

The  general  characters  of  Sympetalae  are  (1)  a  complete 
cyclic  arrangement  of  the  floral  members,  associated  with  defi- 
nite numbers;  (2)  a  sympetalous  corolla  that  usually  has  a 
common  origin  with  the  stamens;  and  (3)  ovules  with  a  single 
massive  integument  and  a  very  small  nucellus.  The  group  con- 
tains fifty-one  families,  the  number  varying  with  different  au- 
thors, and  about  42,000  species,  or  approximately  two-thirds 
of  the  number  included  in  the  Archichlamydeae.  Eight  alli- 
ances have  been  recognized  by  Engler,"  coordinate  with  the  ten 
alliances  of  Monocotyledons  and  the  twenty-six  alliances  of 
Archichlamydeae,  the  contrast  with  the  latter  group  in  uniform- 
ity of  floral  structure  being  very  striking. 

The  natural  sequence  of  the  alliances  is  much  more  evident 
than  among  the  Archichlamydeae.  The  first  three  alliances  are 
252 


CLASSIFICATION  OF  SYMPETALAE  253 

pentacyclic  and  isocarpic,  while  the  remaining  five  are  tetra- 
cyclic  and  anisocarpic ;  and  of  the  anisocarpic  alliances,  the  first 
three  are  hvpogynous  and  the  last  two  epigynous. 

The  three  pentacyclic  or  isocarpic  alliances  are  certainly 
most  nearly  allied  to  the  Archichlamydeae,  for  among  them  poly- 
petaly  still  occurs,  the  two  cycles  of  stamens  are  characteristic, 
and  occasionally  the  ovule  has  two  integuments.  They  may  be 
regarded  as  lines  from  the  Archichlamydeae  in  which  sympetaly 
has  become  prevalent.  They  are  all  hypogynous  and  actino- 
morphic,  and  the  floral  formula  is  characteristically  sepals  5, 
petals  5,  stamens  5  +  5,  carpels  5.  These  comparatively  primi- 
tive Sympetalae  are  not  numerous,  containing  only  about  3,500 
of  the  42,000  species,  and  hence  they  are  not  the  representative 
Sympetalae. 

I.  ERICALES. — This  includes  the  Clethraceae,  Pirolaceae, 
Lennoaceae,  Ericaceae,  Epacridaceae,  and  Diapensiaceae,  to- 
gether containing  a  little  more  than  1,700  species,  by  far  the 
largest  family  being  Ericaceae  with  about  1,360  species.  The 
group  is  characteristically  developed  in  high  latitudes  and  alti- 
tudes, and  its  special  features  are  well  marked.  The  stamens 
are  usually  quite  free  from  the  petals,  and  this  in  connection 
with  occasional  polypetaly  gives  a  strong  resemblance  to  the 
Archichlamydeae ;  while  the  peculiar  dehiscence  of  the  anthers 
and  their  frequent  appendages  are  very  characteristic.  The 
stamens  are  by  no  means  constantly  in  two  cycles,  or  distinct 
from  the  corolla  or  one  another.  A  single  cycle  of  functional 
stamens  may  be  associated  with  staminodia,  or  only  a  single 
cycle  may  appear,  or  the  stamen  cycle  may  have  a  common  ori- 
gin with  the  corolla,  or  in  some  cases  it  may  be  monadelphous. 
In  short,  there  are  transition  forms  to  the  suppression  of  a  cycle 
of  stamens,  and  to  a  common  origin  of  stamen  cycle  and  corolla. 
A  multilocular  ovary  with  numerous  ovules  is  also  a  feature  of 
the  alliance. 

The  Epacridaceae,  a  well-developed  Australian  family  of 
heath-like  plants  containing  nearly  300  species,  are  quite  ex- 
ceptional in  having  only  one  cycle  of  stamens  and  anthers  with 
longitudinal  dehiscence.  These  exceptions  seem  quite  funda- 
mental, but  they  may  be  illustrations  of  the  result  of  long  and 
distant  separation  of  allied  families.  In  any  event,  a  com- 
parative morphological  study  of  Epacridaceae  and  Ericaceae 


254  MORPHOLOGY  OF  ANGIOSPERMS 

is  much  needed ;  and  the  whole  series  of  Ericales  deserves  atten- 
tion on  account  of  its  possible  genetic  connections  with  some 
region  of  the  Archichlamydeae. 

II.  PHIMULALES. — This  includes  the  Myrsinaceae,  Primula- 
ceae,  and  Plumbaginaceae,  together  containing  about  850  spe- 
cies, approximately  equally  distributed  among  the  three  fami- 
lies.     The   families   are   closely   associated    in    structure,    but 
widely  separated  in  geographical  distribution,  the  Myrsinaceae 
being  characteristically  tropical  trees  and  shrubs  (chiefly  Amer- 
ican), the  Primulaceae  north  temperate  and  boreal  herbs,  and 
the  Plumbaginaceae  characteristically  halophytic  herbs  and  un- 
dershrubs  of  salt-beaches  and  steppes   (chiefly  Mediterranean 
and  Caspian).     That  such  dissociated  families  should  have  so 
much  in  common  is  a  strong  argument  against  the  older  idea 
that  similarity  of  structure  proves  common  origin. 

The  two  most  characteristic  features  of  the  group  are  the 
single  cycle  of  stamens  opposite  the  petals,  and  the  unilocular 
ovary  with  its  "  free  central  placenta  "  bearing  numerous  ovules. 
The  single  cycle  of  stamens  and  its  opposition  to  the  petals  are 
explained  by  the  frequent  occurrence  of  rudiments  representing 
an  outer  abortive  cycle.  The  "  free  central  placenta  "  of  tax- 
onomists  is  of  course  a  continuation  of  the  floral  axis  to  bear 
ovules,  and  is  perhaps  the  most  important  morphological  char- 
acter of  the  series.  It  is  in  this  group,  also,  that  there  has  been 
noted  a  peculiar  origin  of  the  petals,  wThich  are  said  to  arise 
late  from  the  primordia  that  have  already  developed  the 
stamens. 

As  compared  with  the  Ericales,  the  Primulales  may  be  re- 
garded as  somewhat  more  advanced  toward  the  higher  Sympeta- 
lae,  but  polypetaly  still  occurs  among  them,  and  they  give  the 
impression  of  a  somewhat  divergent  and  specialized  group.  An 
investigation  of  the  Myrsinaceae  will  doubtless  result  in  a  much 
clearer  understanding  of  the  relationships. 

III.  EBENALES. — This  includes  the  Sapotaceae,  Ebenaceae, 
Styracaceae,  and  Symplocaceae,  together  containing  nearly  900 
species,  the  large  families  being  Sapotaceae  with  about  380  spe- 
cies, and  Ebenaceae  with  275.     The  group  is  chiefly  developed 
in  the  tropics  and  the  species  are  all  shrubs  or  trees. 

The  alliance  is  particularly  puzzling  in  its  affinities,  since 
there  is  a  combination  of  primitive  and  advanced  characters. 


CLASSIFICATION  OF  SYMPETALAE  255 

The  primitive  characters  are  the  indefiniteness  in  the  number 
of  sepals  and  petals,  ranging  from  4  to  8,  occasional  polypetaly, 
and  the  often  numerous  stamens  and  carpels.  Consistency 
would  seem  to  demand  that  the  Ebenales  be  regarded  as  the 
most  primitive  of  the  Sympetalae,  even  the  definite  cyclic  num- 
bers not  being  established.  At  the  same  time,  there  is  adherence 
of  a  single  stamen  cycle  to  a  sympetalous  corolla,  and  distinct 
epigyny.  The  stamen  cycles  are  peculiarly  fluctuating,  ranging 
from  three  or  four  cycles,  through  all  stages  of  suppression  of 
the  outer  cycles,  to  a  single  opposed  cycle.  This  latter  feature  is 
suggestive  of  the  Primulales,  but  the  multilocular  ovary  with 
usually  large  solitary  ovules  is  suggestive  neither  of  Primulales 
nor  Ericales.  The  tropical  forms  certainly  deserve  careful  mor- 
phological investigation,  and  are  doubtless  related  to  the  Myr- 
sinaceae,  and  in  our  judgment  are  to  be  included  in  any  discus- 
sion of  the  most  primitive  Sympetalae. 

In  the  five  following  alliances  the  tetracyclic  character  seems 
to  be  well  established,  and  the  prevailing  formula  is  sepals  5, 
petals  5,  stamens  5,  carpels  2.  In  the  three  previous  isocarpic 
alliances  there  is  every  transition  from  the  pentacyclic  to  the 
tetracyclic  condition,  and  among  the  more  primitive  anisocarpic 
families  the  carpels  are  often  three  before  two  becomes  the 
established  number.  Of  the  remaining  alliances  the  first  three 
are  hypogynous. 

IV.  GEXTIAXALES.* — This  includes  the  Oleaceae,  Salvado- 
raceae,  Loganiaceae,  Gentianaceae,  Apocynaceae,  and  Asclepia- 
daceae,  together  containing  about  4,200  species,  the  large  fami- 
lies being  Asclepiadaceae  with  about  1,720  species,  Apocyna- 
ceae  with  975,  and  Gentianaceae  with  725. 

With  this  alliance  the  grouping  into  developmental  lines 
becomes  indefinite  and  perplexing,  for  the  numerous  families 
intergrade  in  every  direction.  There  is  no  distinctive  character 
that  separates  this  alliance  from  the  great  alliance  Tubiflorales. 
The  fact  that  the  corolla  is  generally  twisted  in  aestivation 
seems  to  be  the  most  useful  character,  and  has  suggested  a  name 
for  the  series,  and  the  constantly  opposite  leaves  is  a  supple- 
mentary character. 

The  lower  members  of  the  alliance  are  the  Oleaceae  and 

*  COXTOBTAE  of  Engler. 


256  MORPHOLOGY  OF  ANGIOSPERMS 

Salvadoraceae,  in  which  there  is  sometimes  distinct  polypetaly, 
but  the  reduction  of  the  stamens  to  two  in  the  former  family 
is  hardly  to  be  regarded  as  a  primitive  character.  The  Logania- 
ceae  are  general  in  their  resemblances,  having  features  in  com- 
mon with  the  remaining  families,  and  others  suggestive  of  Tu- 
biflorales  and  Eubiales.  In  fact,  Engler  suggests  that  the 
Loganiaceae  may  be  an  older  type  than  any  of  the  others,  and 
may  have  given  rise  to  the  Gentianales  and  Rubiales,  in  which 
he  might  have  included  the  Tubiflorales.  If  this  family  may 
hold  any  such  position  in  reference  to  these  great  alliances  it 
certainly  deserves  careful  investigation.  The  alliance  ends  with 
the  Apocynaceae  and  Asclepiadaceae,  in  which  a  latex-system 
is  developed,  and  other  evidences  of  high  specialization  occur; 
but  they  are  also  characterized  by  distinct  carpels,  a  feature  re- 
garded as  primitive.  The  Asclepiadiaceae  form  a  very  peculiar 
and  highly  specialized  offshoot,  the  elaboration  of  floral  struc- 
tures for  entomophily  reaching  a  degree  of  complexity  only  to 
be  compared  with  that  of  the  Orchidaceae. 

V.  TUBIFLORALES.* — This  includes  Convolvulaceae,  Pole- 
moniaceae,  Hydrophyllaceae,  Borraginaceae,  Verbenaceae,  La- 
biatae,  Nolanaceae,  Solanaceae,  Scrophulariaceae,  Bignoniaceae, 
Pedaliaceae,  Martyniaceae,  Orobanchaceae,  Gesneraceae,  Colu- 
melliaceae,  Lentibulariaceae,  Globulariaceae,  Acanthaceae, 
Myoporaceae,  and  Phrymaceae,  together  containing  over  14,600 
species,  the  large  families  being  Labiatae  with  nearly  3,000 
species,  Scrophulariaceae  with  2,400,  Acanthaceae  with  nearly 
2,000,  Solanaceae  with  about  1,700,  and  Borraginaceae  with 
about  1,550. 

This  enormous  assemblage  of  forms  has  been  ordinarily  con- 
sidered as  representing  at  least  two  alliances,  the  Polemoniales 
or  Tubiflorae  including  the  first  four  families  of  the  list  above, 
and  the  Personales  or  Labiatiflorae  including  the  remaining 
families.  The  tendencies  of  development  are  so  numerous  and 
interwoven  that  they  are  difficult  to  separate,  but  rather  than 
merge  two  such  alliances  together  it  might  have  been  better  to 
have  broken  up  the  Personales  into  five  or  six  alliances,  espe- 
cially if  the  Plantaginaceae  are  to  be  set  off  as  a  coordinate 
alliance  Plantaginales.  To  distinguish  them  definitely  would 

*  TUBIFLORAE  of  Engler. 


CLASSIFICATION  OF  SYMPETALAE  257 

probably  be  impossible,  but  an  alliance  at  best  expresses  only  a 
general  evolutionary  tendency  more  or  less  completely  worked 
out. 

Taking  the  alliance  as  a  whole,  it  represents  the  culmination 
of  liypogynous  Sympetalae,  and  this  culmination  is  shown  not 
only  in  the  conspicuous  corolla  but  in  highly  developed  zygo- 
morphism.  In  fact,  the  Personales,  with  the  Labiatae  and 
Scrophulariaceae  as  centers  of  aggregation,  represent  the  great 
zygomorphic  group  of  the  Sympetalae,  as  Leguminosae  do 
among  the  Archichlamydeae,  and  Orchidaceae  among  the  Mono- 
cotyledons. 

First  in  the  alliance  are  the  Convolvulaceae  and  Polemonia- 
ceae  on  account  of  their  actinomorphic  flowers  and  several- 
ovuled  carpels,  in  these  and  other  features  being,  together  with 
the  Gentianales,  the  least  modified  of  the  tetracyclic  families. 
From  Gentianales  they  are  easily  distinguished  by  their  lack 
of  twisted  aestivation  and  by  their  usually  alternate  leaves,  and 
also  by  their  undoubted  relation  to  the  other  families  of  Tu- 
biflorales. 

A  second  natural  alliance  is  that  formed  by  the  Hydrophyl- 
laceae  and  Borraginaceae,  which  leads  from  the  preceding  alli- 
ance through  Hydrophyllaceae,  with  a  generally  unlobed  ovary, 
to  the  Borraginaceae  with  a  much  modified  ovary.  In  the  latter 
family  the  two  carpels  are  divided  by  a  false  partition,  each 
loculus  contains  a  single  ovule,  and  the  ovary  becomes  so  deeply 
lobed  as  to  resemble  a  group  of  four  nutlets.  Further  modi- 
fications of  this  peculiar  fruit,  familiar  to  taxonomists,  make 
it  the  most  specialized  and  diversified  structure  of  this  large 
family. 

A  third  natural  alliance  is  that  formed  by  the  Yerbenaceae 
and  Labiatae,  with  about  3,700  species.  It  is  joined  to  the 
Convolvulaceae  by  the  orientation  of  the  ovule,  and  has  fol- 
lowed a  developmental  path  parallel  with  that  of  the  preceding 
alliance  in  the  evolution  of  the  carpel  structures.  The  lobing 
of  the  ovary  into  four  nutlet-like  bodies  in  the  Labiatae,  how- 
ever, is  not  accompanied  by  such  detailed  specialization  as  in 
the  Borraginaceae ;  but  the  whole  line  is  dominated  by  the 
strong  development  of  zyo-omorphy,  reaching  its  culmination  in 
certain  groups  of  the  Labiatae. 

A  fourth  natural  alliance,  the  greatest  of  all,  includes  the 


258  MORPHOLOGY  OF  ANGIOSPERMS 

eleven  families  from  Xolanaceae  to  Globulariaceae,  grouping 
about  the  Solanaceae  and  Scrophulariaceae.  This  series  con- 
nects with  the  Convolvulus  forms  through  the  Nolanaceae,  but 
does  not  develop  its  carpel-structures  as  do  the  Borrage  and 
Labiate  lines,  retaining  capsules  with  numerous  ovules,  but 
there  is  a  strong  development  of  zygomorphy. 

To  summarize  at  this  point,  the  primitive  stock  of  the  series 
seems  to  be  the  Convolvulaceae-Polemoniaceae  alliance,  from 
which  three  distinct  lines  of  development  have  diverged:  the 
Hydrophyllaceae-Borraginaceae  line,  with  its  modified  carpel- 
structures;  the  Verbenaceae-Labiatae  line,  with  its  modified 
carpel-structures  and  zvgomorphy ;  and  the  Solanaceae-Globu- 
lariaceae  line?  with  its  zygomorphy.  It  should  be  noted  in  pass- 
ing that  the  zygomorphy  is  associated  with  a  strong  tendency 
to  reduce  the  number  of  stamens. 

The  three  remaining  families  are  so  peculiar  in  certain  fea- 
tures that  Engler  regards  them  as  representing  separate  lines  of 
development,  although  the  Acanthaceae  are  not  easily  separated 
from  certain  families  of  the  last  alliance.  The  Myoporaceae 
seem  to  be  a  reduced  type  with  no  clear  affinities;  and  the 
Phrymaceae,  with  their  achenes  and  orthotropous  ovules,  have 
no  evident  connections  in  this  alliance,  in  which  their  strong 
zygomorphy  has  retained  them. 

It  would  be  our  judgment,  therefore,  to  break  up  this  great 
alliance  of  Tubiflorales  into  at  least  four,  which  might  be  called 
the  Polemoniales  ( Convolvulaceae  and  Polemoniaceae),  Bor- 
raginales  (Hydrophyllaceae  and  Borraginaceae),  Labiatales 
(Verbenaceae  and  Labiatae),  and  Personales  (Solanaceae, 
Solanaceae,  Scrophulariaceae,  Bignoniaceae,  Acanthaceae,  Pe- 
daliaceae,  Martyniaceae,  Orobanchaceae,  Gesneriaceae,  Colu- 
melliaceae,  Lentibulariaceae,  and  Globular iaceae),  the  Myo- 
poraceae and  Phrymaceae  being  left  undetermined  or  regarded 
as  reduction  forms  of  Personales. 

VI.  PLANTAGINALES. — This  includes  the  single  family 
Plantaginaceae  with  about  200  species.  This  family,  with  its 
peculiar  habit,  4-merous  flowers,  membranous  corolla,  and  char- 
acteristic fruit,  is  certainly  entitled  to  special  consideration. 
If  such  a  series  as  Tubiflorales  be  maintained,  however,  there 
is  no  good  reason  why  Plantaginaceae  should  not  form  one  of 
the  seven  or  eight  sections  of  it.  If,  on  the  other  hand,  the 


CLASSIFICATION  OF  SYMPETALAE  259 

series  be  broken  up  as  suggested  above,  Plantaginales  should 
certainly  be  coordinate  with  Polemoniales,  Borraginales,  Labi- 
atales,  and  Personales. 

The  two  remaining  alliances  are  epigynous  and  naturally 
form  the  culmination  of  the  Sympetalae.  In  both  alliances  there 
is  actinomorphy  and  numerous  ovules,  but  in  both  there  is  more 
or  less  development  of  zygomorphy;  a  tendency  to  reduction 
in  numbers  of  members,  especially  of  the  ovules;  and  a  tend- 
ency to  reduce  the  flowers  in  size  and  to  mass  them,  leading 
to  a  modification  of  floral  structures  and  a  differentiation  of 
the  functions  of  individual  flowers. 

VII.  RUBIALES. — This  includes  the  Rubiaceae,  Caprifolia- 
ceae,  Adoxaceae,  Valerianaceae,  and  Dipsaceae,  together  con- 
taining nearly  4,800  species,  the  large  family  being  Rubiaceae 
with  nearly  4,100  species. 

The  possible  relationship  of  this  alliance  to  the  Gentianales, 
especially  the  Loganiaceae,  has  been  mentioned,  from  which 
it  seems  to  be  an  epigvnous  offshoot.  At  the  same  time,  rela- 
tions to  the  epigvnous  Umbellales  among  the  Archichlamydeae 
are  no  less  evident.  It  may  possibly  be  found,  as  intimated  in 
the  last  chapter,  that  the  Umbellales  should  be  associated  with 
the  Rubiales  as  two  parallel  alliances  of  epigvnous  Sympetalae. 
Through  the  Caprifoliaceae  the  Valerianaceae  and  Dipsaceae 
are  closely  connected  with  the  alliance ;  while  the  position  of  the 
Adoxaceae  is  altogether  uncertain.  The  distinguishing  char- 
acter to  separate  Rubiales  from  the  next  alliance  is  not  always 
clear,  but  in  general  the  connivent  and  often  united  anthers  of 
the  Campanales  are  not  present  in  the  Rubiales ;  but  this  char- 
acter is  fortified  by  distinct  developmental  tendencies. 

VIII.  CAMPAXALES. — This    includes    the    Cucurbitaceae, 
Campanulaceae,    Goodeniaceae,    Candolleaceae,    Calyceraceae, 
and  Compositae,  together  containing  more  than  14,500  species, 
fully  12,500  of  which  are  Compositae,  the  Campanulaceae  con- 
taining nearly  1,100. 

Connivent  and  often  united  anthers,  and  sometimes  mona- 
delphous  stamens,  prevail  in  the  series.  The  peculiar  tropical 
Cucurbitaceae  occupy  a  special  place  in  the  alliance,  and  can  not 
be  related  clearly  to  the  others ;  while  the  Campanulaceae  seem 
to  represent  a  remnant  of  the  ancient  stock  of  the  alliance,  from 
which  the  other  families  have  arisen. 


260  MORPHOLOGY  OF  AXGIOSPEKMS 


The  alliance  culminates  in  the  Compositae,  the  greatest  of  all 
angiospermous  families,  not  only  in  rank,  but  also  in  the  num- 
ber of  species,  although  not  much  exceeding  the  Leguminosae 
in  this  latter  regard.  There  seems  to  be  no  question  that  the 
Compositae  represent  the  highest  expression  of  the  various  de- 
velopmental lines  we  have  been  tracing  through  the  Angio- 
sperms.  This  is  shown  not  merely  in  their  combination  of 
sympetaly,  epigyny,  and  seed-like  fruit,  but  also  by  such  special 
structures  as  the  pappus  and  the  syngenesious  anthers,  by  the 
complex  organization  of  the  head,  the  prevalence  of  diclinism, 
the  dimorphism  of  corollas,  etc. 


CHAPTER    XIII 

GEOGRAPHIC   DISTRIBUTION   OF   ANGIOSPERMS 

So  vast  a  subject  can  be  presented  only  in  very  brief  outline 
in  a  single  chapter.  In  a  certain  sense  it  is  not  pertinent  to 
a  discussion  of  the  special  morphology  of  a  group,  but  the  stu- 
dent of  special  morphology  is  aided  by  certain  general  consid- 
erations connected  with  geographic  distribution,  especially  in 
any  discussion  of  phylogeny.  The  distribution  of  a  group  con- 
taining nearly  125,000  species  includes  a  vast  mass  of  details, 
and  only  certain  salient  features  can  be  selected  for  presenta- 
tion. Even  when  these  are  selected,  the  numerous  exceptions 
to  any  general  statement  must  be  disregarded.  It  must  be  un- 
derstood, therefore,  that  in  the  following  account  the  statements 
are  very  general  in  their  nature,  expressing  average  conditions 
of  distribution,  under  all  of  which  exceptions  may  be  cited. 
At  the  same  time,  it  is  the  general  tendency  in  the  distribution 
of  any  large  group  that  is  of  interest  to  the  morphologist  rather 
than  the  details  of  distribution  of  species  and  genera. 

The  subject  of  geographic  distribution  presents  two  aspects 
for  consideration.  One  involves  the  determination  of  life-zones 
over  the  surface  of  the  earth,  which  is  a  consideration  of  dis- 
tribution from  the  standpoint  of  physiography.  The  other 
aspect  disregards  the  life-zones,  and  considers  distribution  from 
the  standpoint  of  plant-groups.  What  a  given  plant-group  has 
been  able  to  do  in  the  occupation  of  the  earth's  surface  is  of 
more  morphological  interest  than  the  physiographic  features 
of  the  problem,  and  hence  the  following  presentation  will  take 
the  latter  standpoint. 

Including  only  the  existing  vegetation  gives  a  very  inade- 
quate conception  of  the  relation  of  any  group  to  the  earth's 
surface.  The  present  distribution  of  a  group  is  only  the  last 

^ 


262  MORPHOLOGY  OF  ANGIOSPERMS 

stage  In  a  long  history  of  distribution,  and  a  knowledge  of  this 
history  is  an  essential  factor  in  any  explanation  of  the  present 
distribution.  Unfortunately,  very  little  of  this  history  is  avail- 
able, and  this  presentation  must  content  itself  with  indicating 
the  present  relation  of  groups  to  the  earth's  surface,  without 
any  attempt  at  explanation.  This  is  particularly  unfortunate, 
since  a  lack  of  historical  evidence  may  vitiate  many  conclu- 
sions. If  this  lack  of  historical  testimony  be  added  to  the 
lack  of  any  adequate  record  of  the  geographic  distribution  of 
existing  species,  it  becomes  evident  that  the  generalizations  pro- 
posed must  be  of  the  most  tentative  character.  With  this  ex- 
planation the  following  statements  may  be  given  their  proper 
weight. 

MONOCOTYLEDONS 

It  is  possible  to  present  the  distribution  of  the  ten  alliances 
of  Engler  in  the  order  of  their  supposed  relationship,  a  method 
that  may  be  of  service  in  the  subsequent  consideration  of  the 
ancient  history  and  phylogeny  of  the  group.  One  genetic  group 
is  supposed  to  include  the  three  following  alliances. 

PANDANALES. — The  Pandanaceae  (screw-pines),  apparently 
the  most  primitive  of  Monocotyledons,  belong  to  the  general 
region  of  the  Indian  Ocean.  Associated  with  them  in  relation- 
ship are  the  Typhaceae,  found  in  aquatic  conditions  throughout 
the  world,  but  most  abundant  in  the  tropics ;  and  the  Spargania- 
ceae,  restricted  to  the  temperate  and  boreal  regions  of  the 
northern  hemisphere  and  also  of  the  Australasian  region,  and 
not  represented  in  the  tropics.  The  series  as  a  whole  shows 
wide  adaptations  to  temperature,  but  not  to  soil  conditions,  with 
the  primitive  forms  massed  in  the  oriental  tropics. 

PALMALES. — The  Palmaceae  are  about  equally  divided  be- 
tween the  oriental  and  occidental  tropics,  with  no  temperate 
outliers,  but  not  a  species  or  a  genus  is  common  to  the  two 
hemispheres.  The  geographical  association  of  the  palms  and 
screw-pines  in  the  orient  is  in  favor  of  their  supposed  relation- 
ship, but  the  palms  of  the  Occident  need  explanation,  especially 
since  Phytelephas,  regarded  as  a  genus  intermediate  between 
Pandanaceae  and  Palmaceae,  is  an  American  genus.  The  pres- 
ent distribution  of  palms  is  an  excellent  illustration  of  the  de- 
velopment of  continental  diversities,  which  in  this  case  has 


GEOGRAPHIC  DISTRIBUTION  OF  AXG10SPERMS          263 

resulted  not  only  in  distinct  genera,  but  almost  every  tribe  is 
either  oriental  or  occidental.  Furthermore,  the  much  larger 
number  of  monotypic  genera  in  the  orient  must  be  associated 
with  its  larger  and  more  broken  tropical  area. 

SYXAXTHALES. — The  Cyclanthaceae  are  as  restricted  to 
the  American  tropics  as  the  Pandanaceae  are  to  the  oriental 
tropics. 

If  this  general  "  palm  "  type,  comprising  these  three  alli- 
ances-,  was  once  connected  in  the  two  hemispheres  by  a  northern 
distribution,  the  palms  alone  found  both  hemispheres  congenial 
in  the  tropics,  while  the  Pandanaceae  disappeared  from  the 
western  and  the  Cyclanthaceae  from  the  eastern  hemisphere. 

HELOBIALES. — This  primitive  series  is  very  widely  dis- 
tributed and  contains  relatively  few  species,  probably  on 
account  of  its  aquatic  character.  Three  of  its  families  (Pota- 
mogetonaceae,  Xaiadaceae,  and  Hydrocharitaceae)  have  a 
world-wide  distribution.  The  remaining  five  families  are  some- 
what restricted  as  follows :  Aponogetonaceae  in  the  Indian 
Ocean  region,  Triuridaceae  in  the  tropics  of  both  hemispheres, 
Butomaceae  extending  from  the  tropics  into  temperate  regions, 
while  Juncaginaceae  and  Alismaceae  are  mostly  outside  of  the 
tropics  in  the  northern  and  southern  hemispheres. 

AEALES. — The  possible  relationship  of  this  group  to  the  pre- 
ceding one  has  been  mentioned.  The  aquatic  Lemnaceae  are 
universally  distributed,  but  92  per  cent  of  the  Araceae  are 
within  the  tropics,  being  massed  chiefly  in  South  America, 
India,  and  the  East  Indies.  This  family,  as  the  palms,  affords 
a  good  illustration  of  the  development  of  continental  diversi- 
ties. In  this  case,  however,  the  diversity  has  not  reached  so 
extreme  a  st£ge  as  in  the  palms,  in  which  even  the  tribes  of 
the  orient  and  Occident  are  for  the  most  part  distinct.  Among 
Aroids  the  tribes  of  the  two  hemispheres  are  by  no  means  dis- 
tinct, at  least  two  tropical  genera  (Cyrtosperma  and  Homalo- 
mena)  have  species  in  both  hemispheres,  and  the  monotypic 
Pistia  is  found  in  every  tropical  region.  The  species  are  more 
numerous  in  the  American  tropics,  but  the  number  of  genera 
is  nearly  twice  as  great  in  the  oriental  tropics.  The  Aroids 
differ  further  from  the  palms  in  having  at  least  six  genera 
characteristic  members  of  north  temperate  vegetation,  and  these 
for  the  most  part  are  common  to  both  hemispheres. 
18 


264  MORPHOLOGY  OF  ANGIOSPERMS 

G.LUMALES.— The  world-wide  distribution  of  this  great 
alliance,  from  tropical  to  boreal  conditions,  has  resulted  in  no 
continental  tribes,  comparatively  few  continental  genera,  and 
very  numerous  cosmopolitan  species.  So  far  as  geographic  dis- 
tribution is  concerned,  it  may  well  represent  the  primitive 
stock  from  which  the  following  alliances  have  branched. 

FAKIXALES. — This  alliance  is  made  up  of  a  remarkable  group 
of  isolated  families,  apparently  being  poorly  adapted  for  cos- 
mopolitan distribution.  Only  three  of  the  eleven  families  have 
a  more  extensive  distribution  than  a  hemisphere,  Eriocaula- 
ceae,  the  most  cosmopolitan  family,  being  massed  in  the  tropics, 
Commelinaceae  occurring  everywhere  except  in  boreal  condi- 
tions, and  Pontederiaceae  being  represented  in  all  warmer  re- 
gions. Four  families  (Flagellariaceae,  Restionaceae,  Centro- 
lepidaceae,  and  Rapateaceae)  belong  to  the  southern  hemi- 
sphere, three  (Mayacaceae,  Xyridaceae,  and  Bromeliaceae)  are 
restricted  to  the  western  hemisphere,  and  Philydraceae  are 
Australian. 

LILIALES. — This  series,  in  contrast  to  the  Farinales,  is  made 
up  of  characteristically  cosmopolitan  families.  Liliaceae  and 
Iridaceae  are  literally  cosmopolitan,  Amaryllidaceae  and  Tac- 
caceae  are  massed  in  all  tropical  regions,  Juncaceae  are  best  de- 
veloped in  the  cool  temperates  of  the  northern  and  southern 
hemispheres,  Haemodoraceae  are  represented  in  tropical  Amer- 
ica and  Australia,  Stemonaceae  are  scattered  in  patches  in 
Australia,  Asia,  and  North  America,  and  Dioscoreaceae  are 
mainly  tropical.  Only  Velloziaceae  are  restricted  to  a  single 
hemisphere,  and  the  restriction  is  remarkable,  since  all  of  the 
*70  species  are  credited  only  to  Brazil. 

SCITAMINALES. — The  four  families  of  this  series  are  all 
tropical,  two  of  them  (Musaceae  and  Zingiberaceae)  being  re- 
stricted to  the  oriental  tropics,  and  two  (Cannaceae  and  Maran- 
taceae)  to  the  occidental. 

OECHIDALES. — The  massing  of  orchids  in  the  tropics  of  -both 
hemispheres  is  well  known,  but  they  are  by  no  means  restricted 
to  tropical  conditions.  As  a  rule,  the  numerous  tropical  genera 
are  not  only  restricted  to  hemispheres,  but  are  often  very  local ; 
while  the  temperate  genera  are  represented  in  both  hemi- 
spheres, and  the  most  northern  genera  even  contain  cosmopoli- 
tan species. 


GEOGRAPHIC  DISTRIBUTION  OF  ANGIOSPERMS          265 

Upon  examining  such  data,  certain  generalizations  in  refer- 
ence to  the  distribution  of  Monocotyledons  become  apparent. 
These  will  doubtless  be  modified  by  a  fuller  knowledge  of  the 
distribution  of  families,  but  they  will  serve  to  illustrate  certain 
facts : 

1.  Four  great  terrestrial  families  (Gramineae,  Cyperaceae, 
Liliaceae,   and  Iridaceae)    of  Monocotyledons  are  world-wide 
in  their  distribution.     This  means  that  they  have  been  able  to 
become  adapted  to  every  condition  of  soil  and  climate  possible 
to  high-grade  vegetation. 

2.  The  Monocotyledons   include   a  remarkable  number  of 
purely  hydrophytic  families  which  also  have  a  world-wide  dis- 
tribution so  far  as  fresh  and  brackish  waters  are  concerned. 
The  families  are   Typhaceae,  Potarnogetonaceae,   Xaiadaceae, 
Hydrocharitaceae,    Lemnaceae,    and    Pontederiaceae,    four    of 
them  belonging  to  the  Helobiales.     In  spite  of  this  wide  dis- 
tribution, these  families  contain  less  than  200  species.     When 
this  fact  is  taken  in  connection  with  the  10,000  species  belong- 
ing to  the   four   cosmopolitan   terrestrial   families   mentioned 
above,  it  becomes  evident  that  the  very  diverse  conditions  of  the 
land  surface  are  far  more  favorable  to  the  production  of  species 
than  the  comparatively  uniform  aquatic  conditions. 

3.  There  is  a  decided  massing  of  monocotyledonous  families 
in  the  tropics.     This  is  so  marked  as  to  suggest  that  Monocotyle- 
dons as  a  whole  are  essentially  tropical. 

4.  As  a  corollary  to  the  last  statement,  the  entire  absence 
of  boreal  forms,  excepting  the  few  belonging  to  the  families 
of  universal  distribution,  is  noteworthy. 

5.  The    poor    representation    of    Monocotyledons    in    the 
southern    hemisphere,    exclusive    of    the   world-wide    families, 
is  remarkable.     Especially  is  this  true  of  Australia,  a  region 
prolific  in  endemic  forms  among  Gymnosperms  and  Dicotyle- 
dons. 

6.  Very  few  families  are  characteristic  of  temperate  re- 
gions, and  these    (Sparganiaceae,  Juncaginaceae,  Alismaceae, 
and   Juncaceae)    are   represented    in   both   the   northern    and 
southern  hemispheres,   and  none  of  them  are  of  the  higher 
petaloideous  type. 

7.  The   tropical  representation   of   Monocotyledons   is   ap- 
proximately equal  in  the  two  hemispheres,  not  merely  in  num- 


266  MORPHOLOGY  OF  ANGIOSPERMS 

her  of  species  but  also  of  families.  The  tropical  families  repre- 
sented in  both  hemispheres  are  Butomaceae,  Triuridaceae, 
Palmaceae,  Araceae,  Eriocaulaceae,  Commelinaceae,  Amaryl- 
lidaceae,  Taccaceae,  Dioscoreaceae,  Burmanniaceae,  and  Orchi- 
daceae.  Those  peculiar  to  the  oriental  tropics  are  Pandanaceae, 
Aponogetonaceae,  Musaceae,  and  Zingiberaceae.  Those  peculiar 
to  the  occidental  tropics  are  Cyclanthaceae,  Mayacaceae,  Xyri- 
daceae,  Bromeliaceae,  Haemodoraceae,  Velloziaceae,  Canna- 
ceae,  and  Marantaceae. 

8.  The   great    preponderance    of    epiphytic    forms    in    the 
American  tropics  is  probably  associated  with  the  culmination 
of  the   rainy  forest.      The  two  great  epiphytic   families   are 
Bromeliaceae  and  Orchidaceae,  the  former  being  restricted  to 
the  occidental  tropics,  and  the  latter  much  more  abundant  there 
than  in  the  oriental  tropics. 

9.  The  peculiar  distribution  of  the  three  genera  of  Stemona- 
ceae  is  noteworthy  and  suggestive.     Stemona,  with  four  or  five 
species,    ranges   from   the    Himalayas    to    southern    Australia. 
Croomia  has  one  of  its  species  (C.  pauciflora)  in  Florida,  Geor- 
gia, and  Japan;  while  the  other  (C.  japonica)  is  restricted  to 
Japan.     The  monotypic  Stichneuron  is  restricted  to  the  East 
Indies.      The  occurrence   of  a   single   species  of  this   oriental 
family  in  Georgia  and  Florida,  and  that  species  native  also  to 
Japan,  is  difficult  to  explain. 

AKCHICHLAMYDEAE 

It  is  impossible  to  consider  the  geographic  distribution  of 
the  Archichlamydeae  in  such  detail  as  that  of  the  Monocotyle- 
dons. The  series  are  so  numerous  and  indefinite  that  a  presen- 
tation of  their  separate  distribution  wrould  be  confusing  and 
not  very  significant.  An  examination  of  available  but  very 
insufficient  data  has  resulted  in  the  following  extremely  general 
statements : 

1.  Xo  family  has  developed  a  world-wide  distribution  as 
have  several  families  of  the  Monocotyledons  and  Sympetalae. 
It  must  be  understood  that  this  fact  is  related  to  the  great 
diversities  in  the  group,  that  have  resulted  in  the  recognition 
of  numerous  families.  The  family  differences  recognized  by 
taxonomists  are  perhaps  not  to  be  pressed  too  far  in  any  com- 
parison of  the  geographic  distribution  of  the  three  great  Angio- 


GEOGRAPHIC  DISTRIBUTION  OF  ANGIOSPERMS          267 

sperm,  groups.  If  they  are  of  equal  value,  the  Archichlamydeae 
respond  more  readily  to  geographic  conditions  than  do  the  other 
groups.  We  suspect,  however,  that  they  are  of  very  unequal 
value,  and  that  the  kind  of  response  shown  by  the  Archichlamy- 
deae to  changed  conditions  happens  to  concern  the  structures 
used  for  determining  families  more  than  in  the  other  groups. 

•2.  Among  the  Archichlamydeae  no  distinctly  boreal  family 
has  been  developed,  as  among  the  Sympetalae. 

3.  The  great  tropical  family  is  the  Leguminosae,  by  far 
the  largest  Angiosperni  family  excepting  the  Compositae.     If 
the  Mimosa  forms  are  to  be  regarded  as  the  primitive  ones,  it  is 
interesting  to  note  that  they  are  massed  in  tropical  Africa  and 
Australia,  and  that  it  is  the  highly  specialized  Papilio  forms 
that  have  chiefly  occupied  the  temperate  regions. 

4.  Certain  great  families  are  characteristic  of  the  north 
temperate  regions,  usually  being  comparatively  insignificant  in 
the   tropics.      These    are   the    Polygonaceae,    Caryophyllaceae, 
Kammculaceae,  Cruciferae,  Saxifragaceae,  Rosaceae,  Onagra- 
ceae,  and  Umbelliferae. 

5.  As  among  the  Monocotyledons,  aquatic  forms  are  com- 
mon and  cosmopolitan,   but  this  habit  does  not  characterize 
whole  families  so  frequently  as  in  the  former  group.     The  fact 
that  the  aquatic  habit  is  found  chiefly  among  the  Monocotyle- 
dons and  Archichlamydeae  must  be  associated  with  the  fact  that 
in  these  groups  the  most  primitive  Angiosperms  occur.     The 
cosmopolitan  character  of  such  forms  may  be  illustrated  by 
the   Ceratophyllaceae,   which  with   only  three  species  extends 
from  the  arctic  to  the  antarctic  regions,  occurring  even  in  Aus- 
tralia and  the  Fiji  Islands. 

6.  There  is  a  distinct  pairing  of  continents  especially  in 
tropical  display,  as  was  noted  among  the  Monocotyledons,  in 
this  case  America  usually  being  one  member  of  the  pair  and 
Asia  or  Africa  the  other.     In  this  pairing,  what  may  be  called 
the   Pacific-distribution,   involving   Asia,   the   East   Indies,   or 
Australia  on  the  one  hand,  and  the  Americas  on  the  other,  is 
particularly  prominent.     For  example,  the  Amarantaceae  are 
massed  in  South  America  and  the  East  Indies,  the  Lardiza- 
balaceae  in  South  America  and  southeastern  Asia,  the  Calycan- 
thaceae  in  Xorth  America  and  Japan,  the  Lauraceae  in  Amer- 
ica and  Asia,  the  Malvales  chiefly  in  America  and  Asia,  the 


268  MORPHOLOGY  OF  ANGIOSPERMS 

Myrtaceae  in  South  America  and  Australia,  etc.  This  pairing 
is  still  more  evident  if  closely  related  families  are  included,  as 
the  Sarraceniaceae  in  North  America  and  the  Nepenthaceae  in 
tropical  eastern  Asia  and  the  East  Indies.  The  pairing  of 
Australia  and  Africa  is  less  notable,  as  the  Mimosa  tribe,  massed 
in  tropical  Australia  and  Africa,  and  the  Thymelaeaceae,  chiefly 
occurring  in  temperate  Australia  and  the  Cape  region.  The 
pairing  of  America  and  Africa,  or  the  Atlantic-distribution, 
is  quite  rare. 

7.  The  predominance  of  the  American  tropics  in  the  devel- 
opment of  Archichlamydeae  is  marked,  as  might  be  inferred 
from  the  last  paragraph,  almost  all  of  the  tropical  groups  being 
represented  there,  and  two  great  families  (Cactaceae  and  Melas- 
tomaceae)  being  almost  exclusively  American. 

8.  As  might  be  expected,  there  is  a  much  greater  display  of 
Archichlamydeae  in  the  north  temperate  regions  than  in  the 
south.     Two  large  families,  however,  are  characteristic  of  the 
south  temperate  regions — namely,  the  Proteaceae,  chiefly  Aus- 
tralian, some  South  African,  and  a  few  South  American ;  and 
the  Thymelaeaceae,  characteristic  of  Australia  and  the  Cape 
region. 

9.  It  is  of  interest  to  note  that  the  dominant  tree-groups, 
so  characteristic  of  Archichlamydeae,  are  of  different  alliances 
in  the  different  regions.     For  example,  in  north  temperate  re- 
gions the  Juglandales,  Fagales,  etc.,  dominate;  in  the  tropics 
the  Lauraceae  are  the  characteristic  tree-forms ;  while  in  south 
temperate   regions   the   Proteaceae    are   the    prominent    archi- 
chlamydeous  forest  trees. 

10.  There  is  a  notable  diffusion  of  types  into  all  regions, 
so  that  very  few  families  are  restricted  in  their  representation, 
although  most  of  them  have  a  fairly  definite  region  of  massing. 
Characteristic  tropical  families  have  representatives  in  the  tem- 
perate regions,  and  families  chiefly  developed  in  the  temperate 
regions  have  tropical  representatives. 

SYMPETALAE 

The  alliances  of  Sympetalae  are  comparatively  so  few  and 
well  defined  that  they  may  be  considered  separately. 

EKICALES. — This  alliance  is  peculiar  in  containing  distinct- 
ly temperate  and  boreal  forms.  It  includes  an  arctic  family 


GEOGRAPHIC  DISTRIBUTION  OF  ANGIOSPERMS          269 

(Diapensiaceae),  an  Australian  family  (Epacridaceae),  and  a 
great  massing  of  heath-forms  in  the  Cape  region. 

PEIMULALES. — The  three  families  are  very  distinct  in  their 
geographic  distribution,  Myrsinaceae  being  tropical,  especially 
American,  Primulaceae  north  temperate  and  boreal,  and 
Plumbagmaceae  characteristically  oriental  in  the  halophytic 
conditions  of  the  Mediterranean  and  Caspian  regions. 

EBEXALES. — The  alliance  is  almost  exclusively  tropical,  and 
in  both  hemispheres. 

GEXTIAXALES. — The  alliance  as  a  whole  is  more  largely 
massed  in  the  tropics  through  the  tropical  display  of  its  largest 
families,  Apocynaceae  and  Asclepiadaceae.  It  contains  also  a 
great  liana  group  (Loganiaceae)  characteristic  of  South  Amer- 
ica and  Asia,  and  there  is  a  pairing  of  Africa  and  Asia  by 
the  Salvadoraceae.  The  Gentianaceae  have  almost  a  world- 
wide distribution,  but  are  notable  in  their  numerous  alpine 
species. 

TUBIFLOEALES. — This  great  series  is  in  the  main  broken 
up  into  fairly  well-restricted  areas,  and  the  chief  features  of 
their  distribution  may  be  stated  as  follows :  The  Labiatae  are 
world-wide  in  their  distribution,  being  notably  massed  in  the 
Mediterranean  region.  The  Borraginaceae  and  Scrophularia- 
ceae  are  the  great  north  temperate  families.  The  Solanaceae 
are  everywhere  in  the  tropics,  extending  into  temperate  regions 
especially  in  America.  The  Convolvulaceae,  Polemoniaceae, 
and  Hydrophyllaceae  are  characteristically  American,  the  first 
being  chiefly  tropical,  and  the  other  two  characteristic  of  west- 
ern Xorth  America.  The  Gesneraceae  belong  to  all  regions 
of  the  southern  hemisphere ;  while  the  Yerbenaceae,  Xolana- 
ceae,  and  Acanthaceae  are  notably  in  tropical  South  America. 
There  are  also  two  Mediterranean  families,  the  Orobanchaceae 
and  Globulariaceae.  The  pairing  of  South  America  and  Asia 
is  shown  in  the  display  of  Yerbenaceae  and  Acanthaceae;  and 
of  tropical  Asia  and  Africa  in  the  display  of  Pedaliaceae. 

PLAXTAGIXALES. — The  genus  Plantago  is  cosmopolitan. 

RUBIALES. — The  Rubiaceae  are  prominently  tropical  Amer- 
ican ;  the  Caprifoliaceae  and  Valerianaceae  are  north  temper- 
ate throughout  both  hemispheres :  while  the  Dipsaceae  seem 
to  be  confined  to  the  temperate  regions  of  the  eastern  hemi- 
sphere. 


270  MORPHOLOGY  OF  ANGIOSPERMS 

CAMPAN  ALES. — The  Cucurbitaceae  are  tropical ;  the  Cam- 
panulaceae  belong  to  the  north  and  south  temperate  regions, 
with  the  lobelias  as  tropical  representatives;  the  Goodeniaceae 
and  Candolleaceae  are  Australian ;  the  Calyceraceae  are  mainly 
tropical  American ;  and  the  Compositae  are  world-wide  in  their 
distribution. 

The  main  conclusions  to  be  derived  from  the  above  facts  are 
as  follows : 

1.  The  Sympetalae  as  a  whole  are  better  defined  geograph- 
ically than  the  Archichlamydeae.     This  probably  follows  from 
the  fact  that  they  are  better  defined  structurally. 

2.  There  is  a  much  more  even  distribution  between  the 
tropics  and  temperates  than  among  the  Monocotyledons  and 
Archichlamydeae.     Of  course  the  tropical  display  is  the  larger, 
but  it  is  hardly  more  than  might  be  regarded  as  the  normal 
ratio    of    increase    in    passing    from    the    temperates    to    the 
tropics. 

3.  The  Sympetalae  as  a  whole,  the  youngest  of  the  Angio- 
sperm  groups,  seem  to  have  become  prominently  adapted  to  the 
relatively  unoccupied  temperate  and  boreal  conditions,  and  to 
have  made  in  them  their  most  characteristic  display.     From 
this   general   point   of  view,   the   Monocotyledons   and   Archi- 
chlamydeae are  characteristically  tropical,  and  the  Sympetalae 
as  characteristically  temperate. 

4.  There  is  a  remarkable  paucity  of  aquatic  forms  as  com- 
pared  with   Monocotyledons   and    Archichlamydeae.      This    is 
probably  associated  W7ith  at  least  two  facts — namely,  the  lack 
of  primitive  angiospermous  types  among  the  Sympetalae,  and 
the  previous  occupation  of  the  water  conditions  by  the  older 
Monocotyledons  and  Archichlamydeae. 

5.  The  Sympetalae  show  no  such  notable  continental  pair- 
ing as  is  characteristic  of  the  Archichlamydeae.     It  would  seem 
that  this  may  be  related  to  the  temperate  and  boreal  develop- 
ment of  the  group,  which  would  retain  continental  connections 
much  longer  than  would  be  possible  for  a  group  of  more  tropical 
tendencies. 

6.  The  dominance  of  America  in  the  tropical  display  of 
Sympetalae  is  almost  as  notable  as  among  the  Archichlamydeae. 
The  excessive  rainfall  is  doubtless  one  factor  in  the  explana- 
tion, but  whether  it  is  the  chief  one  is  uncertain. 


GEOGRAPHIC  DISTRIBUTION  OF  AXGIOSPERMS          271 

7.  The  sympetalous  families  of  world-wide  distribution  are 
the  Compositae,  Labiatae,  and  Plantaginaceae. 

8.  The  great  north  temperate  families  are  the  Borragina- 
ceae  and  Scrophulariaceae. 

9.  The  characteristic  boreal  group  is  the  Ericales,  a  group 
that  finds  no  parallel  among  the  Monocotyledons  and  Archi- 
chlamydeae. 


CHAPTEK    XIV 

FOSSIL   ANGIOSPEBJVJS 

THE  importance  of  a  knowledge  of  the  ancient  history  of 
Angiosperms  can  not  be  overestimated.  The  morphological 
conclusions  as  to  phylogeny  that  can  be  confirmed  by  historical 
evidence  rest  upon  the  securest  available  foundation.  Unfor- 
tunately, the  paleobotanical  record  of  Angiosperms  is  very  frag- 
mentary and  poorly  understood.  The  published  accounts  are 
dominated  mainly  by  stratigraphy  rather  than  by  plant-groups, 
and  the  named  material  is  often  so  uncertain  as  to  its  affinities 
that  the  morphologist  is  extremely  perplexed  in  drawing  any 
conclusions.  Even  when  all  data  are  rejected  excepting  those 
that  rest  upon  reasonably  secure  botanical  evidence,  any  con- 
clusions must  be  extremely  tentative,  not  only  because  much 
of  the  evidence  is  negative,  but  also  because  much  of  the  re- 
jected material  undoubtedly  contains  valuable  testimony.  In 
spite  of  this  uncertainty,  it  may  be  useful  to  put  together  such 
testimony  as  we  possess.  Even  this  may  modify  some  concep- 
tions as  to  phvlogeny. 

MONOCOTYLEDONS 

When  the  parallel  venation  of  leaves  was  taken  to  be  a  dis- 
tinctive character  of  the  Monocotyledons  their  presence  in  the 
Carboniferous  was  claimed.  But  since  it  has  become  known 
that  such  leaves  are  equally  characteristic  of  the  great  Paleozoic 
group  Cordaites,  as  well  as  of  other  Gymnosperms,  and  of  cer- 
tain heterosporous  Pteridophytes,  this  claim  rests  upon  no  sub- 
stantial basis.  So  far  as  we  have  been  able  to  examine  the 
testimony,  it  must  be  said  that  the  existence  of  Paleozoic  Mono- 
cotyledons has  not  been  proved. 

There  is  no  historical  evidence  that  the  Monocotyledons 
have  ever  been  a  dominant  race,  as  the  Gymnosperms  have 
272 


FOSSIL  ANGIOSPERMS  273 

been,  and  as  the  Dicotyledons  now  are,  although  they  do  not 
seem  to  be  so  abundant  now  as  they  were  during  the  Tertiary. 
When  they  do  appear  in  undoubted  forms,  they  are  almost  com- 
pletely differentiated  and  widely  distributed.  Their  ancestral 
forms  are  obscured  in  the  maze  of  unintelligible  forms  that  pre- 
cede them.  The  only  suggestion  of  paleobotany  as  to  the  origin 
of  the  Monocotyledons  is  that  they  are  certainly  a  younger  type 
than  the  Gymnosperms. 

Rejecting  the  claim  for  Carboniferous  Monocotyledons,  we 
encounter  one  for  their  existence  during  the  Jurassic.  This 
rests  upon  the  occurrence  of  certain  forms  of  grass-like  habit, 
which  suggest  Monocotyledons,  but  such  evidence  can  not  be 
accepted  as  conclusive.  There  is  certainly  no  clear  proof  of  the 
existence  of  Monocotyledons  in  any  strata  earlier  than  the  Cre- 
taceous.* 

The  probability  of  Monocotyledons  during  the  Jurassic  rests 
not  upon  positive  discovery,  but  upon  the  fact  that  during  the 
Cretaceous  they  were  abundant  everywhere,  and  give  evidence 
of  their  long  presence.  The  earliest  history  of  the  group, 
therefore,  is  an  absolute  blank,  and  we  are  introduced  to  it  in 
an  advanced  stage  of  development. 

The  record  can  be  considered  under  three  general  catego- 
ries— namely,  (1)  those  families  represented  during  the  Cre- 
taceous, (2)  those  whose  earliest  representatives  are  in  the  Ter- 
tiary, and  (3)  those  only  known  since  the  Tertiary.  It  must 
be  observed  that  the  second  and  third  categories  are  based  upon 
negative  evidence- — that  is,  representatives  of  these  families 
have  not  been  found  as  yet  at  any  earlier  period.  It  must  also 
be  remembered  that  many  plants  have  a  habitat  and  structure 
unfavorable  to  their  preservation  as  fossils,  so  that  failure  to 
discover  them  in  the  geological  series  is  no  positive  evidence 
that  they  did  not  exist.  With  the  uncertainties  understood  it 
may  be  safe  to  present  such  evidence  as  we  have. 

CRETACEOUS  FAMILIES. — There  seems  to  be  sure  evidence 
of  the  existence  of  five  families  during  the  Cretaceous,  and  a 
possibility  of  the  occurrence  of  a  sixth. 

The   Pandanaceae  were  present   and  were  widely  distrib- 

*  See  SEWARD,  A.  C. :  Xotes  on  the  Geological  History  of  Monocotyledons. 
Annals  of  Botany  10:  205-220.  pi.  U.     1896. 


274  MORPHOLOGY  OF  ANGIOSPERMS 

uted.  This  fact  seems  to  substantiate  the  claim  as  to  the  primi- 
tive character  of  this  family,  and  to  discount  the  theory  of  its 
origin  as  a  reduction  type.  Xot  only  did  the  screw-pine  exist, 
but  the  family  was  richer  in  forms  than  at  present,  all  the 
living  genera  containing  more  numerous  species  than  now,  and 
at  least  one  extinct  genus  having  been  recognized. 

A  little  later  in  the  Cretaceous  the  Palmaceae  occurred 
abundantly,  but  in  genera  that  are  now  for  the  most  part 
extinct.  Their  distribution  wras  very  wide-spread,  remains  hav- 
ing been  found  in  deposits  from  Greenland  to  Egypt.  This 
early  association  of  Pandanaceae  and  Palmaceae  is  corrobora- 
tive of  the  idea  of  their  genetic  relationship,  and  the  later  ap- 
pearance of  the  Palmaceae  further  confirms  the  morphological 
evidence  that  they  may  have  been  derived  from  the  Panda- 
naceae. 

The  Potamogetonaceae  were  abundant,  a  fact,that  coincides 
well  with  their  morphological  position  as  the  most  primitive 
of  the  Helobiales,  and  controverts  the  idea  that  they  are  a 
reduced  type.  That  they  were  more  abundantly  displayed  dur- 
ing the  Cretaceous  than  now7  is  evidenced  by  the  fact  that  the 
majority  of  our  present  genera  were  represented,  and  at  least 
three  extinct  genera  have  been  detected. 

The  above  families  would  be  expected  by  a  morphologist  to 
occur  among  the  earliest  Monocotyledons,  but  the  Cretaceous 
record  also  discloses  the  presence  of  the  Liliaceae.  However, 
they  are  comparatively  few  in  number,  occur  in  the  upper  mem- 
bers of  the  Cretaceous  series,  and  do  not  fairly  display  them- 
selves until  the  Tertiary,  when  numerous  and  now  extinct  gen- 
era appeared.  These  earlier  liliaceous  forms  are  of  the  Smilax 
type,  but  this  negative  evidence  is  very  uncertain,  as  this  type 
is  peculiarly  favorable  for  preservation. 

The  Dioscoreaceae  also  appeared  along  with  the  Liliaceae, 
and  are  so  confused  with  the  Smilax  forms  as  to  be  difficult 
to  disentangle. 

The  sixth  family,  whose  existence  during  the  Cretaceous  is 
possible  but  far  from  certain,  is  the  Araceae,  to  which  certain 
doubtful  forms  have  been  referred.  It  may  have  been  scantily 
represented,  and  its  association  with  the  Potamogetonaceae 
would  be  confirmatory  of  Engler's  suggestion  as  to  their  genetic 
connection. 


FOSSIL  ANGIOSPERMS  275 

TERTIARY  FAMILIES. — To  the  five  monocotyledoncms  fami- 
lies represented  during  the  Cretaceous  the  Tertiary  adds  at  least 
fourteen,  the  older  families  also  showing  a  largely  increased 
development.  It  will  be  interesting  to  note  how  these  addi- 
tional families  fill  out  the  ten  great  series  of  Monocotyledons. 
In  each  case  the  Cretaceous  representative  is  put  in  paren- 
thesis. 

1.  Pandanales. — (Pandanaceae),  Typhaceae,  Spargania- 
ceae.  This  primitive  series  is  thus  completed  as  at  present 
recognized. 

-2.  II  el  ob  idles. — (Potamogetonaceae),  Juncaginaceae,  Buto- 
maceae,  Hydrocharitaceae.  This  series  is  completed  by  the 
appearance  of  its  highest  member,  and  the  Butomaceae  are 
fairly  representative  of  the  Alismaceae. 

3.  Glumales. — Gramineae,  Cyperaceae.  The  occurrence  of 
irra— -like  forms  during  the  Jurassic  has  been  referred  to,  but 
the  absence  of  grasses  from  the  Cretaceous  record  seriously 
militates  against  the  claim  that  these  Jurassic  forms  were 
grasses.  It  is  since  the  Tertiary  that  the  Gramineae  have  be- 
come most  richly  developed  and  widely  spread,  numerous  ex- 
tinct genera  having  been  described.  Although  it  would  seem 
impossible  to  determine  the  relationships  of  grasses  from  frag- 
mentary material,  and  doubt  must  be  expressed  as  to  the  rela- 
tionships implied  in  such  names  as  Poacites,  Arundinites,  etc., 
there  is  good  evidence  for  the  statement  that  the  earliest  grass 
types  were  related  to  such  tropical  forms  as  Arundo,  Phrag- 
mites,  Bambusa,  etc. 

-i.  Pal  males. — (Palmaceae).  The  only  family  of  the  series 
became  much  more  largely  developed  and  wide-spread  during 
the  Tertiary. 

5.  Synanthales. — Cyclanthaceae.      This    family,    the    only 
member  of  the  series,  appeared  during  the  Eocene  Tertiary, 
and  its  early  association  with  the  screw-pines  and  palms  con- 
firms its  supposed  relationship  to  them. 

6.  Amies. — (Araceae?).     The  doubtful  appearance  of  this 
family  during  the  Cretaceous  has  been  mentioned,   and  this 
claim  is  not  helped  by  the  fact  that  they  are  no  better  known 
during  the  Tertiary.     Such  forms  as  do  occur  resemble  Acorns 
and  Pistia.     The  so-called  "  Protolemnas  "  seem  too  doubtful 
to  be  included. 


276  MORPHOLOGY  OF  ANGIOSPERMS 

7.  Farinales. — Restionaceae,    Centrolepidaceae,   Eriocaula- 
ceae.     Three  of  the  eleven  families  of  the  series  are  thus  intro- 
duced, the  first  two  now  being  restricted  to  the  southern  hemi- 
sphere, but  during  the  Tertiary  ranging  through  Europe. 

8.  Liliales. — (Liliaceae,  Dioscoreaceae),  Juncaceae,  Irida- 
ceae.     The  last  family  is  the  highest  member  of  the  series,  and 
its  appearance  before  certain  of  the  lower  families  is  altogether 
doubtful. 

9.  Scitaminales. — Musaceae.     The  series  consists  of  four 
families,  and  this  one,  now  confined  to  the  oriental  tropics,  is 
recognized  as  the  most  primitive. 

10.  Orcliidales. — Xot  represented.  , 
At  the  end  of  the  Tertiary,  therefore,  there  is  reasonable 

evidence  as  to  the  existence  of  all  the  great  Aeries  of  Monocoty- 
ledons excepting  the  highest,  and  of  nearly  one-half  the  fam- 
ilies. 

DICOTYLEDONS 

Any  evidence  as  to  the  comparative  antiquity  of  Monocoty- 
ledons and  Dicotyledons  is  much  to  be  desired,  but  as  yet  the 
historical  evidence  is  not  definite,  for  no  undoubted  Monocoty- 
ledon has  been  recorded  from  strata  older  than  those  in  which 
typical  Dicotyledons  first  occur,  and  vice  versa.  The  great  and 
sudden  prominence  of  the  Dicotyledons  in  the  Upper  Cretaceous 
and  Tertiary  was  long  a  puzzle,  only  relieved  by  the  solitary 
Populus  primaeva  of  the  Lower  Cretaceous.  Comparatively 
recent  studies,  however,  of  contemporaneous  beds  in  the  United 
States  and  Portugal  now  regarded  as  Lower  Cretaceous  have 
thrown  much  light  upon  the  subject,  and  since  1888  our  knowl- 
edge of  the  origin  of  the  Dicotyledons  has  increased  rapidly. 
It  should  be  remembered  that  the  group  is  largely  composed  of 
herbaceous  plants,  and  could  not  have  a  fair  representation 
among  fossil  forms. 

LOWER  CRETACEOUS  DICOTYLEDONS. — The  dicotyledonous 
flora  of  the  Lower  Cretaceous  was  an  abundant  one,  and  is  of 
great  interest  in  the  history  of  Dicotyledons.  It  consists  of  a 
plexus  of  forms,  some  of  which  are  clearly  related  to  existing 
Dicotyledons,  others  are  clearly  Dicotyledons  but  with  no  living 
representatives,  while  others  are  vague  in  their  relationship  to 
Dicotyledons.  The  few  forms  that  can  be  referred  with  any 


FOSSIL  AXGIOSPER3IS  277 

definiteness  to  modern  groups  are  fairly  submerged  by  the  ex- 
tinct and  vague  types.  Such  a  plexus  is  consistent  with  any 
evolutionary  theory  of  the  origin  of  Dicotyledons,  and  that  it 
has  been  definitely  discovered  in  the  Lower  Cretaceous  is  of 
great  importance. 

Proangiosperms. — These  are  the  vague  forms  referred  to 
above  as  being  not  definitely  Dicotyledons  but  suggestive  of 
them.  They  are  recognized  by  stem-structure  and  leaf-vena- 
tion, and  seem  to  be  related  to  numerous  modern  families, 
being  good  illustrations  of  so-called  "  comprehensive  types." 
It  is  hardly  to  be  doubted  that  many  of  them  represent  primi- 
tive Dicotyledons.  If  the  Lower  Cretaceous  be  divided  into 
five  periods,  the  Proangiosperms  not  suggestive  of  modern 
groups  are  the  only  dicotyledonous  forms  in  the  first.  In 
the  other  periods  they  also  occur,  but  in  diminishing  impor- 
tance as  compared  with  the  increasing  number  of  recognizable 
forms.  These  clearly  antecedent  and  for  a  time  associated 
forms  are  very  suggestive  of  their  significant  relation  to  modern 
Dicotyledons. 

Forms  suggestive  of  Modern  Groups. — After  the  first  period 
of  the  Lower  Cretaceous,  forms  suggestive  of  modern  groups 
appear.  They  are  so  clearly  Dicotyledons  as  not  to  be  included 
among  the  Proangiosperms,  but  they  are  just  as  distinctly  not 
modern  types.  Their  generic  names  suggest  the  modern  resem- 
blances, but  these  must  not  be  taken  to  indicate  relationships. 
For  example,  such  names  as  Leguminosites,  Menispermites, 
Myrsinophyllum,  Proteophyllum,  Peucedanites,  etc.,  tell  of  cer- 
tain superficial  resemblances,  but  may  be  very  far  from  indi- 
cating real  relationships. 

Modern  Genera. — As  already  stated,  no  modern  genera  were 
associated  with  the  Proangiosperms  during  the  first  period  of 
the  Lower  Cretaceous.  In  the  second  period,  however,  an  ex- 
tinct species  of  Popidus  has  been  recognized,  the  most  ancient 
living  genus  of  Dicotyledons  known.  In  the  third  period  Mag- 
nolia and  Liriodendron  are  recorded;  in  the  fourth  Salix,  Aris- 
tolochia,  Sassafras,  Adoxa,  and  Aralia  appeared;  and  in  the 
fifth  Myrica,  Laurus,  Eucalyptus,  and  Viburnum  are  recorded. 

In  considering  this  record  of  the  Lower  Cretaceous  the  fol- 
lowing things  become  evident : 

1.  The  genera,  so  far  as  they  are  identical  with  living  gen- 


278  MORPHOLOGY  OF  ANGIOSPERMS 

era,  are  practically  all  members  of  the  Archichlamydeae.  The 
case  of  Viburnum,  and  even  of  Aralia,  is  peculiar,  and  perhaps 
suggestive  of  a  far  more  complete  development  of  the  Dicoty- 
ledons than  the  records  have  shown. 

2.  The  early  appearance  of  Populus  confirms  the  general 
primitive   character   of   naked   flowers   and   the   anemophilous 
habit. 

3.  Xone  of  the  known  chalazogamic  forms  are  represented 
in  the  above  list,  so  that  chalazogamy  can  hardly  be  regarded 
as  a  primitive  character,  as  has  been  claimed,  unless  it  be  as- 
sumed that  these  earlier  genera  were  chalazogamic  and  later 
became  porogamic. 

4.  Of  the  twelve  modern  genera  represented  in  the  list,  no 
less  than  eight  are  recognized  by  morphologists  as  primitive 
in  character. 

5.  The  occurrence  of  one  of  the  Sympetalae  in  the  upper- 
most member  of  the  Lower  Cretaceous,  and  that  an  epigynous 
form,  needs  explanation.     It  leads  to  at  least  one  of  three  con- 
clusions.    Either  the  determination  is  a  mistake,  or  a  large 
representation  of  sympetalous  genera  remain  to  be  discovered 
in  the  Lower  Cretaceous,  or  the  present  view  as  to  the  relative 
rank  and  phylogeny  of  sympetalous  families  must  be  modified. 
If  the  determination  of  Viburnum  is  the  correct  one,  its  associa- 
tion with  Aralia  is  confirmatory  of  a  genetic  connection  which 
we  have  long  maintained. 

6.  That  epigyny  had  appeared  among  the  undoubted  Archi- 
chlamvdeae during  the  Lower  Cretaceous  is  seen  by  the  exist- 
ence of  such  a  genus  as  Eucalyptus. 

UPPER  CRETACEOUS  DICOTYLEDONS. — Much  less  is  known 
of  the  flora  of  the  Upper  Cretaceous  than  of  the  Lower  Creta- 
ceous. There  must  have  been  a  large  development  of  existing 
genera,  such  as  Salix,  Populus,  and  Liriodendron  being  well 
known,  as  well  as  an  introduction  of  new  ones. 

TERTIARY  DICOTYLEDONS. — The  record  of  the  dicotyledo- 
nous flora  of  the  Tertiary  is  naturally  made  up  of  the  trees  and 
shrubs.  The  forest  display  was  evidently  as  extensive  and  va- 
ried as  now.  In  addition  to  the  genera  mentioned  above,  all  of 
which  show  increasing  development,  there  appeared  the  Betula- 
ceae,  Fagaceae,  Juglandaceae,  Moraceae,  Proteaceae,  Berberi- 
daceae,  Staphyleaceae,  Aceraceae,  etc.  This  means  an  almost 


FOSSIL  ANGIOSPERMS  279 

complete  display  of  the  more  primitive  Archichlamydeae.  A 
notable  introduction  during  the  Tertiary  was  that  of  the  Legu- 
iiiinosae.  That  these  appeared  first  only  as  Mimosa  forms  is  a 
strong  confirmation  of  the  primitive  character  of  this  tribe,  -as 
well  as  <>f  its  possible  relation  to  the  Rosaceae. 

The  above  facts  in  reference  to  the  early  history  of  the  Di- 
cotyledons seem  to  warrant  the  following  conclusions: 

1.  The  modern  Dicotyledons  were  derived  from  a  plexus  of 
vague  forms  developed  largely  in  the  Lower  Cretaceous  and 
known  as  Proangiosperms. 

'2.  The  Cretaceous  and  Tertiary  display  is  almost  exclu- 
sively made  up  of  Archichlamydeae,  the  dominant  types  being 
the  more  primitive  Archichlamydeae. 

3.  The  Sympetalae  are  practically  absent  from  the  Creta- 
ceous and   Tertiary,  and  represent  therefore  a  comparatively 
recent  type. 

4.  The  possible  appearance  of  Viburnum,  associated  with 
Aralia,  at  the  close  of  the  Lower  Cretaceous  suggests  a  connec- 
tion of  L^mbellales  with  the  Sympetalae  not  recognized  by  tax- 
onomistfi. 

5.  Xone  of  the  highly  specialized  groups  of  the  Arehichla- 
mydeae  are  represented  in  the  Cretaceous  and  Tertiary,  such  a 
family  as  the  Leguminosae  being  represented  by  its  most  primi- 
tive type,  and  all  the  types  being  what  may  be  called  "  compre- 
hensive." 

6.  The  identity  of  genera  in  the  eastern  and  western  hemi- 
spheres indicates  the  absence  of  continental  diversities,  which 
later  became  so  striking  a  feature  in  geographical  distribution. 

7.  The  theory  that  simple  flowers  are  necessarily  reduced 
rather  than  primitive  structures  seems  to  have  a  complete  refu- 
tation in  the  testimony  of  history. 


CHAPTER    XV 

PHYLOGENY   OF  ANGIOSPERMS 

THE  phylogeny  of  any  great  group  will  probably  always 
remain  a  baffling  problem.  At  the  same  time,  theories  of  phy- 
logeny serve  to  coordinate  knowledge  and  stimulate  investiga- 
tion. The  phylogeny  of  Angiosperms  is  an  unusually  obscure 
problem.  The  hypotheses  proposed  seem  to  include  almost 
every  possibility,  but  thus  far  they  have  been  more  interesting 
than  convincing.  When  similarity  of  structure  was  taken  as  a 
sure  indication  of  genetic  relationships,  the  problem  promised 
an  approximate  solution.  But  since  it  has  been  proved  that 
similar  structures  may  develop  independently,  the  difficulty  of 
solution  has  apparently  become  insurmountable.  Under  such 
circumstances  it  is  questionable  whether  a  discussion  of  the  sub- 
ject is  profitable,  but  a  statement  of  the  problem  may  not  be 
out  of  place. 

The  first  phase  of  the  problem  has  to  do  with  the  common 
or  independent  origin  of  the  Monocotyledons  and  Dicotyledons. 
It  has  been  assumed  generally  that  the  two  groups  are  mono- 
phyletic.  The  chief  argument,  and  in  fact  the  only  morpholog- 
ical one  for  the  monophyletic  theory,  lies  in  the  great  uni- 
formity of  the  peculiar  development  of  both  the  male  and 
female  gametophytes.  It  is  argued  that  the  independent 
origin  of  such  exact  details  of  development  and  structure 
is  inconceivable,  and  this  argument  has  been  reenforced  re- 
cently by  the  discovery  in  both  groups  of  the  peculiar  phe- 
nomenon called  "  double  fertilization."  The  argument  is  cer- 
tainly a  very  strong  one,  and  yet  there  are  rebutting  proposi- 
tions. Even  such  similarity  in  structure  may  be  the  natural 
outcome  of  the  changes  that  resulted  in  the  evolution  of  seeds, 
and  these  are  now  generally  believed  to  have  appeared  in  inde- 
280 


PHILOGENY  OF  AXGIOSPERMS  281 

pendent  lines.  Again,  the  fundamental  differences  in  the  de- 
velopment of  the  embryos  of  the  two  groups  are  hard  to  recon- 
cile upon  the  theory  of  monophyletic  origin.  Add  to  this  the 
fundamental  differences  in  the  structure  of  the  stem  and  in 
the  character  of  its  vascular  bundles,  and  the  derivation  of  one 
group  from  the  other  seems  more  inconceivable  than  the  deriva- 
tion of  the  Dicotyledons  from  the  Gymnosperms.  Still  another 
argument  against  the  monophyletic  theory  is  furnished  by  the 
historical  testimony.  The  Proangiosperms  of  the  Lower  Cre- 
taceous, so  far  as  known,  appeared  associated  with  undoubted 
Monocotyledons,  and  merged  gradually  into  recognizable  Di- 
cotyledons, without  indicating  any  relationship  to  the  Mono- 
cotyledons. The  emerging  of  Dicotyledons  from  this  vague 
group  either  indicates  that  Monocotyledons  and  Dicotyledons 
originated  independently,  or  that  the  Proangiosperms  were 
transition  forms  between  Monocotyledons  and  Dicotyledons. 
This  latter  alternative  is  in  turn  .inconceivable,  especially  since 
the  most  primitive  Dicotyledons  are  recognized  to  be  even  more 
primitive  than  any  of  the  Monocotyledons. 

Recently,  however,  the  morphological  arguments  in  favor 
of  the  monophyletic  origin  of  Angiosperms  have  been  reen- 
forced  by  anatomical  investigations,  which  point  to  origin  from 
a  common  proangiospermous  stock,  or  the  derivation  of  the 
Monocotyledons  from  the  more  primitive  Dicotyledons.  In  the 
following  chapters  it  will  be  noted  that  on  anatomical  grounds 
Jeffrey  regards  the  Monocotyledons  as  strictly  monophyletic 
and  modern,  derived  from  the  Dicotyledons  or  their  parent 
stock ;  and  on  the  same  ground  Queva  9  thinks  that  the  Mono- 
cotyledons are  derived  from  the  lower  Dicotyledons.  In  her 
study  of  the  origin  of  the  cotyledon  in  Monocotyledons,  Miss 
Sargant 18  concludes  that  the  Monocotyledons  are  a  specialized 
branch  from  the  Dicotyledons.  In  Anemarrhena,  one  of  the 
Liliaceae,  she  finds  two  opposed  vascular  bundles  in  the  ter- 
minal cotyledon.  These  run  down  into  the  short  hypocotyl, 
where  each  divides  into  two,  and  the  four  phloems  so  formed 
are  continuous  with  those  of  the  tetrarch  primary  root.  This 
suggests  that  two  cotyledons  are  represented,  which  were  sepa- 
rate in  some  dicotyledonous  ancestor.  The  same  investigator 
also  finds  in  Erianthis,  one  of  the  Ranunculaceae,  a  possible 
illustration  of  this  dicotyledonous  ancestor;  for  the  petioles 


282  MORPHOLOGY  OF  ANGIOSPERMS 

of  the  cotyledons  are  united  throughout  their  length,  showing 
two  opposed  bundles,  as  in  the  cotyledon  of  Anemarrliena. 
Attention  should  be  called  to  similar  cotyledonary  tubes  in 
Dicotyledons,  and  since  nearly  all  of  these  are  geophilous  plants 
Miss  Sargant  21  has  inferred  that  the  fused  condition  of  the 
cotyledons  in  the  monocotyledons  has  arisen  in  connection  with 
the  geophilous  habit.  We  herewith  reproduce  Miss  Sargant's 
list  of  dicotyledonous  seedlings  with  a  well-marked  cotyledonary 
tube. 

Anemone  coronaria,  A.  alpina,  A.  blanda,  A.  narcissiflora,  A.  rupi- 
cola,  Ranunculus  parnassifolius,  Trollius  Ledebouri,  Erianthis  hiema- 
lis,  Delphinium  nudicaule,  D.  hybridum  and  vars.,  Aconitum  Anthora, 
Leontice  vesicaria,  L.  altaica,  Podophyllum  peltatum,  P.  Emodi,  Car- 
damine  spp.,  Oxalis  spp.,  Rhizophora  Mangle,  R.  conjugata,  Megar- 
rhiza  californica,  Smyrnium  perfoliatum,  S.  rotundifolium,  S.  Olusa- 
trum,  Bunium  luteum,  Chaerophyllum  bulbosum,  Prangos  ferulacea, 
Serratula  radiata,  Dodecatheon  Meadia,  Polygonum  Bistorta,  P.  sphae- 
rostachyum,  and  Rheum  Moorcroftianum. 

Holm  7  has  also  studied  the  two  completely  united  cotyledons 
of  Podopliyllum,  which  suggested  to  him  the  possibility  that 
the  "  pair  "  may  be  regarded  as  a  single  cotyledon.  In  her 
study  of  the  "  monocotyledonous  Dicotyledons/'  Miss  Sargant  21 
claims  that  the  so-called  single  cotyledon  is  a  fusion  of  two 
cotyledons,  special  reference  being  made  to  the  well-known  case 
of  Ranunculus  Ficaria.  It  may  be  noted  also  that  in  1896 
Delpino 2  urged  the  origin  of  the  monocotyledonous  phylum 
from  Dicotyledons  through  Butomus.  Recently  Hallier,20  bas- 
ing his  phylogeny  upon  sporophylls  and  foliage  leaves  ("  tro- 
phophylls"),  has  urged  the  origin  of  Monocotyledons  from 
Dicotyledons,  claiming  that  they  have  arisen  from  the  region 
of  the  Ceratophyllaceae  and  Ranunculaceae. 

There  can  be  no  question  that  among  the  Xymphaeaceae, 
Ranunculaceae,  and  Berberidaceae  there  occur  anatomical  struc- 
tures very  suggestive  of  Monocotyledons,  as  Campbell 15  has 
recently  pointed  out,  but  that  this  proves  the  origin  of  Mono- 
cotyledons from  Dicotyledons  rather  than  the  reverse  is  not 
evident.  Even  the  evidence  derived  from  cotyledons  has  been 
taken  by  Lyon  14  as  indicating  that  the  dicotyledonous  condi- 
tion has  been  derived  from  the  gradual  splitting  of  the  single 
cotyledon  of  Monocotyledons.  If  the  view  of  the  phylogeny  of 


PHYLOGEXY   OF  AXGIOSPERiffS  283 


the  cotyledon  maintained  by  Lyon  17  be  true  (see  Chapter  IX), 
the  Monocotyledons  are  more  primitive  than  the  Dicotyledons 
and  have  given  rise  to  them. 

It  is  an  old  view,  however,  that  the  Dicotyledons  are  the 
more  primitive,  and  that  the  Monocotyledons  have  been  derived 
from  them  as  a  reduction  series.  Later  the  relatively  primi- 
tive character  of  the  Monocotyledons  was  maintained  without 
serious  opposition.  A  detailed  presentation  of  the  phylogeny 
of  Angiosperms  from  this  point  of  view  may  be  found  in 
Bessey's  3  "  Phylogeny  and  Taxonomy  of  the  Angiosperms." 

In  our  judgment  the  evidence  is  strongly  in  favor  of  the 
independent  origin  of  the  two  groups,  which  have  attained  prac- 
tically the  same  advancement  in  the  essential  morphological 
structures,  but  are  very  diverse  in  their  more  superficial 
features.  Their  great  distinctness  now  indicates  either  that 
they  were  always  distinct  or  that  they  originated  from  forms 
that  were  really  Proangiosperms  and  neither  Monocotyledons 
nor  Dicotyledons.  It  may  be  well  to  state  in  this  connection 
that  in  speaking  of  the  origin  of  one  great  group  from  another, 
the  former  is  not  supposed  to  have  arisen  as  a  single  branch. 
For  example,  to  say  that  Monocotyledons  have  been  derived 
from  Dicotyledons  does  not  imply  that  a  single  monocotyled- 
onous  branch  arose  from  some  definite  group  of  the  Dicotyle- 
dons, but  that  probably  several  monocotyledonous  lines  arose 
from  one  or  more  regions  of  the  Dicotyledons,  regions  that 
may  or  may  not  be  illustrated  by  living  groups. 

The  next  phase  of  the  problem  raises  the  question  whether 
the  Angiosperms  have  been  derived  from  the  Gymnosperms  or 
directly  from  the  Pteridophytes.  The  general  question  is  the 
same  whether  one  believes  in  their  monophyletic  character  or 
not.  The  older  view  is  that  the  Angiosperms  have  been  derived 
from  the  Gymnosperms,  and  Gnetum  has  been  regarded  as  the 
nearest  living  representative  of  a  transition  condition  between 
Gymnosperms  and  Angiosperms.  The  argument  is  based  upon 
certain  resemblances  of  Gnetum  to  the  Angiosperms,  chief 
among  them  being  the  absence  of  archegonia,  the  organization 
of  eggs  while  the  gametophyte  consists  of  free  cells,  the  presence 
of  a  perianth  and  true  vessels,  and  the  Dicotyledon-like  leaves. 
This  showing  is  strong  but  perhaps  not  conclusive.  If  this 
origin  be  maintained,  it  is  evident  not  only  from  the  leaf  char- 


284  MORPHOLOGY   OF  ANGIOSPERMS 

acters,  but  still  more  from  the  nature  of  the  embryo  and  the 
structure  of  the  stem,  that  the  primitive  Angiosperm  stock 
would  be  the  Dicotyledons.  Strasburger  recognized  this  neces- 
sity when  proposing  the  theory,  and  regarded  the  Monocotyle- 
dons as  a  reduced  branch  from  the  Dicotyledons ;  which  is 
another  reenforcement  of  the  argument  derived  from  recent 
anatomical  investigations.  In  fact,  the  Gymnosperm  ances- 
try of  Dicotyledons  also  gains  a  point  in  the  entire  absence 
of  pteridophytic  anatomical  features  in  the  shoots  of  Dico- 
tyledons. 

Lately,  also,  Karsten,16  in  a  morphological  study  of  the 
Juglandaceae,  emphasizes  their  resemblances  to  Gymnosperms, 
and  concludes  that  the  Angiosperms  have  been  derived  from  such 
forms  as  Gnetum.  The  historical  argument  against  such  a  claim 
is  the  absence  of  any  certain  evidence  of  the  existence  of  Gnetum 
among  the  numerous  Angiosperms  of  the  Cretaceous  and  Terti- 
ary. If  it  were  related  in  any  way  to  the  origin  of  such  a  group  as 
the  Angiosperms,  it  seems  probable  that  it  would  have  left  some 
evidence  of  its  existence.  Of  course  this  is  negative  evidence, 
and  remains  of  ancient  Gnetales  may  be  found  in  the  tropics 
or  in  the  southern  hemisphere.  The  argument  from  the  pres- 
ence of  a  perianth  is  particularly  vulnerable,  since  the  so-called 
perianth  merely  represents  the  bracts  common  among  Gymno- 
sperms, and  the  most  primitive  Dicotyledons  and  Monocotyle- 
dons have  no  perianth.  Further,  the  presence  of  true  vessels 
is  an  argument  as  much  in  favor  of  the  origin  of  the  Angio- 
sperms from  certain  heterosporous  Pteridophytes  as  from  Gne- 
tum. Although  we  regard  the  origin  of  Angiosperms  from 
Gymnosperms  as  very  improbable,  the  embryo-sac  structures 
of  Gnetum  are  suggestive  of  the  way  in  which  the  character- 
istic sac-structures  of  the  Angiosperms  may  have  arisen  from 
a  compact  gametophyte.  This  is  all  the  more  probable  since 
the  sac-structures  of  certain  Juglandaceae  and  of  Peperomia 
pellucida  have  been  found  to  be  suggestive  of  those  of  certain 
species  of  Gnetum. 

If  the  Gymnosperms  are  not  the  ancestral  forms  of  the  An- 
giosperms, their  direct  derivation  from  the  Pteridophytes  be- 
comes a  matter  of  course.  The  Pteridophyte  that  has  been  most 
persistently  associated  with  the  origin  of  Angiosperms  is  Isoe- 
tes.  Its  resemblances  to  the  Monocotyledons  have  suggested 


PHYLOGEXY  OF  ANGIOSPERMS  285 

that  it  may  be  the  nearest  living  representative  of  their  ancestral 
forms.  Isoetes  is  a  remarkably  isolated  group  among  the  Pteri- 
dophytes,  with  no  clear  affinities,  so  that  its  own  connection  with 
the  Pteridophyte  stock  is  not  evident.  The  most  striking  re- 
semblance to  Monocotyledons  occurs  in  the  embryo,  in  which 
the  single  cotyledon  is  terminal  and  the  stem-tip  arises  later 
as  a  lateral  structure.  The  development  of  the  male  gameto- 
phyte  resembles  Angiosperms  more  than  it  does  Gymnosperms, 
while  the  female  gametophyte  is  equally  suggestive.  However, 
these  gametophyte.  characters  are  shared  by  Selaginella.  The 
general  habit  and  vegetative  structure  of  Isoetes  bear  some  re- 
semblance to  those  of  an  aquatic  Monocotyledon,  and  the  anat- 
omy of  the  stem  is  suggestive  of  such  forms  as  Yucca  and  Dra- 
caena. There  can  be  no  question  that  the  resemblances  of  Isoe- 
tes to  the  Monocotyledons  are  more  numerous  than  those  of  any 
other  living  Pteridophyte.  The  most  telling  resemblance  is 
the  character  of  the  embryo,  but  the  fact  that  its  axis  is  trans- 
verse to  that  of  the  suspensor  is  a  serious  obstacle.  Campbell 
has  called  attention  to  the  fact,  however,  that  in  the  embryos 
of  Lilaea  subulata  and  Zannichellia  the  apex  of  the  root  is  not 
directed  toward  the  suspensor  but  to  one  side,  so  that,  the  axis 
of  the  embryo  is  oblique  to  that  of  the  suspensor.  A  possible 
explanation  of  these  laterally  directed  roots,  however,  is  sug- 
gested by  Murbeck's  recent  account  of  Ruppia  (page  196),  in 
which  a  primary  root  is  formed  with  the  normal  orientation, 
but  soon  disorganizes,  while  a  lateral  root,  formed  very  early, 
is  the  first  functional  one.  As  between  the  Gnetum  origin 
of  Angiosperms  and  the  Isoetes  origin  of  Monocotyledons  the 
latter  view  must  be  preferred.  Such  a  view,  of  course,  does 
not  imply  that  the  present  Monocotyledons  have  been  derived 
from  the  present  Isoetaceae,  but  that  the  ancestral  forms  of 
the  two  were  probably  genetically  connected.  If  this  be  true, 
doubtless  Isoetes  represents  a  reduced  branch  of  some  old  stock 
that  gave  rise  to  the  more  vigorous  Monocotyledons.  The  only 
possible  alternative  as  to  the  origin  of  Monocotyledons,  in  case 
they  have  arisen  independently  of  the  Dicotyledons,  seems  to 
be  to  regard  them  as  the  end  of  a  heterosporous  line  that 
developed  independently  from  the  eusporangiate  Filicales, 
whose  Pteridophyte  members  are  extinct.  Such  an  hypothesis 
is  only  necessary  in  the  event  that  those  based  upon  known 


286  MORPHOLOGY  OF  ANGIOSPERMS 

structures  prove  to  be  insufficient;  but  the  problem  seems  to 
have  reached  this  contingency  now. 

To  many,  any  conclusion  as  to  the  origin  of  the  Monocoty- 
ledons involves  that  of  the  Dicotyledons,  which  they  would  re- 
gard as  an  ancient  branch  from  the  Monocotyledon  stock.  We 
have  already  cited  reasons  why  such  a  view  does  not  commend 
itself  to  us,  and  prefer  to  regard  Dicotyledons  as  of  independent 
origin.  If  the  two  lines  have  a  common  origin,  it  seems  to  us 
that  the  arguments  in  favor  of  the  derivation  of  Monocotyle- 
dons from  the  more  primitive  Dicotyledons  are  the  more  con- 
vincing. Both  lines  to-day  include  very  primitive  forms,  and 
the  structure  of  the  flower  and  character  of  the  megasporan- 
giate  archesporium  are  more  primitive  among  existing  Dicot- 
yledons than  among  Monocotyledons.  Whether  Dicotyledons 
represent  an  independent  angiospermous  line,  as  we  prefer  to 
believe,  or  the  primitive  Angiosperm  stock,  it  remains  to  dis- 
cuss their  possible  origin.  The  fact  that  they  emerged  from 
a  primitive  group  called  Proangiosperms,  which  was  largely 
developed  in  the  first  period  of  the  Lower  Cretaceous,  seems 
to  be  fairly  well  established  by  paleobotany.  The  question 
thus  concerns  the  origin  of  the  Proangiosperms.  They  do 
not  seem  to  warrant  the  belief  that  they  represent  a  common 
stock  from  which  both  Monocotyledons  and  Dicotyledons  have 
been  derived,  for  the  Monocotyledons  are  believed  to  have  ex- 
isted in  unmistakable  forms  before  the  large  assemblage  of  Pro- 
angiosperms gave  rise  to  unmistakable  Dicotyledons.  Still 
less  conceivable  is  it  that  the  Proangiosperms  represent  the 
transition  forms  from  Monocotyledons  to  Dicotyledons,  for 
.nothing  in  their  known  structure  seems  to  suggest  such  a  view. 
That  they  were  derived  from  Gnetum-\ike  forms  is  discredited 
by  the  fact  that  there  is  no  sure  record  of  the  existence  of 
Gnetum  at  such  an  early  period,  and  to  have  given  rise  to 
such  an  assemblage  of  forms  it  must  have  been  a  conspicuous 
group. 

If  we  turn  to  the  earlier  groups  that  were  sufficiently  prom- 
inent and  at  all  suggestive  of  having  given  rise  to  the  Pro- 
angiosperms, we  encounter  the  Coniferales,  Cycadales,  Lycopo- 
diales,  and  Filicales.  The  Gymnosperm-origin  of  Dicotyledons 
seems  to  be  most  unlikely  with  the  exclusion  of  Gnetum.  At 
the  same  time,  it  might  be  claimed  that  Dicotyledons  represent 


PHYLOGEXY  OF  ANGIOSPERMS  287 

an  independent  line  from  the  Gymnosperm-stock,  that  advanced 
in  the  same  direction  and  much  farther  than  did  the  Gnetum- 
line.  At  the  same  time,  all  the  essential  morphology  of  the 
Gymnosperms  is  less  favorable  to  such  an  origin  than  is  that 
of  the  heterosporous  Pteridophytes. 

The  Lycopodiales  certainly  deserve  serious  consideration  in 
this  connection.  The  structures  of  Selaginella  are  about  as 
suggestive  of  Dicotyledons  as  those  of  Isoetes  are  suggestive 
of  Monocotyledons,  the  embryo  being  as  distinctly  dicotyledo- 
nous as  that  of  Isoetes  is  monocotyledonous,  and  the  seed-like 
character  of  the  megasporangium  supplies  a  still  more  striking 
resemblance.  Such  a  view  does  not  imply  that  the  present  com- 
paratively modern  genus  Selaginella  has  given  rise  to  the  Pro- 
angiosperms,  but  that  the  latter  may  have  been  derived  from 
the  same  ancient  Lycopodium  stock. 

The  only  remaining  alternative  hypothesis  is  that  mentioned 
in  connection  with  the  origin  of  the  Monocotyledons,  namely,  the 
derivation  of  the  Proangiosperms  as  an  independent  heteros- 
poroiW  line  from  the  abundant  ancient  eusporangiate  Filicales, 
and  tnis  view  is  supported  by  anatomical  testimony.  It  may 
be  that  further  knowledge  of  the  Proangiosperms  will  help  to 
establish  such  an  hypothesis. 

It  seems  to  us  that  the  last  two  hypotheses  deserve  the  most 
consideration,  as  likely  to  include  the  future  results  of  investi- 
gation. 

It  should  be  noted  in  connection  with  the  origin  of  Dicoty- 
ledons that  there  is  much  evidence  in  favor  of  the  view  that  they 
include  two  independent  lines.  For  example,  Campbell  inclines 
to  the  view  that  one  line  is  derived  from  the  Arales,  passing 
by  way  of  the  Piperales  and  amentaceous  groups  to  the  isocar- 
pous  Sympetalae,  while  the  other  arises  from  the  apocarpous 
Helobiales,  and  by  way  of  the  Ranales  and  later  groups  cul- 
minates in  the  anisocarpic  Sympetalae.  Although  not  inclined 
to  accept  the  origin  suggested,  the  existence  of  two  such  inde- 
pendent lines  of  Dicotyledons  has  very  much  in  its  favor, 
whether  derived  from  the  Monocotyledons  or  not. 

A  summary  of  our  present  views,  as  developed  in  the  preced- 
ing pages,  may  be  stated  as  follows:  The  Monocotyledons  and 
Dicotyledons  represent  two  independent  lines  derived  directly 
from  Pteridophyte  stock,  probably  from  the  Filicales.  At  the 


288  MORPHOLOGY  OF  ANGIOSPERMS 

same  time,  the  arguments  in  favor  of  the  monophyletic  origin 
of  Angiosperms  are  strong;  and  if  this  view  be  accepted,  the 
derivation  of  Monocotyledons  from  primitive  Dicotyledons 
seems  to  rest  on  stronger  evidence  than  the  reverse  relationship. 
It  must  also  be  said  that  the  Gymnosperm  origin  of  Angio- 
sperms is  not  to  be  discredited  so  much  now  as  formerly. 

The  student  of  the  phylogeny  of  any  group  of  vascular 
plants  should  be  acquainted  with  certain  general  theoretical 
views.  Among  them  the  origin  of  the  sporophytic  generation 
is  one  of  the  most  fundamental.  Two  theories  are  under  dis- 
cussion, known  as  that  of  homologous  origin  and  that  of  anti- 
thetic origin,  names  applied  by  Celakovsky.  According  to  the 
former  theory,  the  sporophyte  is  the  lineal  descendant  of  the 
sexless  individuals  common  among  Thallophytes  and  homolo- 
gous with  the  sexual  individuals;  according  to  the  latter  the- 
ory, the  sporophyte  is  a  new  structure  intercalated  in  the  life 
history  of  plants  and  holding  no  phylogenetic  relation  to  any 
preceding  individuals.  The  theory  of  homologous  origin  is  re- 
ferred to  Pringsheim  in  1876 ;  that  of  antithetic  origin  was 
formulated  by  Celakovsky  in  1877,  but  was  presented  in  detail 
by  Bower  in  1890.  In  1896  the  theory  of  homologous  origin 
was  again  brought  into  prominent  notice  by  Scott  in  a  presi- 
dential address  before  the  British  Association ;  and  two  years 
later  Bower,  upon  a  similar  occasion,  defended  the  theory  of 
antithetic  origin.  A  general  presentation  of  the  subject  by 
Klebs,4  Lang,5  and  Hartog  6  followed,  including  the  testimony 
of  recent  investigations.  Undoubtedly  the  strongest  argument 
in  favor  of  the  homologous  origin  of  the  sporophyte  is  derived 
from  the  phenomena  of  apogamy  and  apospory;  and  among 
Ferns  these  have  been  coming  to  light  so  rapidly  and  are  in- 
duced so  readily  that  the  powers  of  gametophyte  and  sporo- 
phyte, at  least  in  this  group,  seem  to  be  easily  interchangeable, 
a  fact  most  easily  explained  by  their  homologous  character.  It 
will  be  noted  that  in  all  this  discussion  there  is  no  suggestion 
that  sporophytes  may  have  arisen  in  both  of  these  ways,  a  possi- 
bility that  will  be  considered  a  little  later. 

One  of  the  most  suggestive,  theories  of  recent  years  is 
Bower's  l  theory  of  the  strobilus.  ^sTo  better  statement  of  its 
main  points  can  be  made  than  that  of  the  author  himself  in 
his  summary. 


PHYLOGENY   OF   AXGIOSPERMS  289 

1.  Spore-production  was  the  first  office  of  the  sporophyte,  and  the 
spore-phase  has  constantly  recurred  throughout  the  descent  of  the 
Archegoniatae ;  the  spore-bearing  tissues  are  to  be  regarded  as  primary, 
the  vegetative  tissues  as  secondary,  in  point  of  evolutionary  history. 

2.  Other  things  being  equal,  increase  in  number  of  carpospores  is 
an  advantage;  a  climax  of  numerical  spore-production  was  attained 
in  the  homosporous  Vascular  Cryptogams. 

3.  Sterilization  of  potential  sporogenous  tissues  has  been  a  wide- 
spread phenomenon,  appearing  as  a  natural  consequence  of  increased 
spore-production. 

4.  Isolated  sterile  cells  or  layers  of  cells  (tapetum)  served  in  many 
cases  the  direct  function  of  nourishing  the  developing  spores,  being 
themselves  absorbed  during  the  process. 

5.  By  formation  of  a  central  sterile  mass  (columella,  etc.)  the  spore- 
production  was,  in  more  complex  forms,  relegated  to  a  more  superficial 
position. 

6.  In  vascular  plants,  parts  of  the  sterile  tissue  formed  septa,  par- 
titioning off  the  remaining  sporogenous  tissue  into  separate  loculi. 

7.  Septation  to  form  synangia,  and  subsequent  separation  of  the 
sporangia,  are  phenomena  illustrated  in  the  upward  development  of 
vascular  plants. 

8.  Such  septation  may  have  taken  place  repeatedly  in  the  same 
line  of  descent. 

9.  The  strobilus  as  a  whole  is  the  correlative  of  a  body  of  the 
nature  of  a  sporogonial  head,  and  the  apex  of  the  one  corresponds  to 
the  apex  of  the  other. 

10.  Progression  from  the  simpler  to  the  more  complex  type  de- 
pended upon  (a)  septation,  and  (6)  eruption  to  form  superficial  appen- 
dicular  organs  (sporangiophores,  sporophylls)  upon  which  the  sporan- 
gia are  supported. 

11.  By  continued  apical  growth  of  the  strobilus,  the  number  of 
sporophylls  may  be  indefinitely  increased. 

12.  The  sporophylls  are  susceptible  of  great  increase  in  size  and 
complexity  of  form  ;  in  point  of  evolutionary  history,  small  and  simple 
sporophylls  preceded  large  and  complex  ones. 

13.  In  certain  cases  foliage-leaves  were  produced  by  sterilization 
of  sporophylls. 

This  theory  means  that  the  leafy  sporophyte  is  derived  from 
such  a  sporophytic  structure  as  is  displayed  by  the  sporogonium 
of  Bryophytes;  but,  as  suggested  by  Klebs  and  Lang,  it  may 
have  had  an  entirely  independent  origin,  and  may  have  no 
phylogenetic  connection  with  such  a  structure  as  a  sporogonium. 
This  view,  together  with  its  possible  relations  to  the  question 
of  antithetic  versus  homologous  origin  of  the  sporophyte,  has 


290  MORPHOLOGY  OF  AXGIOSPERMS 

been  discussed  by  Coulter,8  the  substance  of  whose  paper  may 
be  stated  in  the  following  extracts : 

It  has  been  common  to  regard  the  distinct  sporophyte  as  having 
been  established  once  for  all  by  the  Bryophytes,  and  the  sporophytes 
of  the  higher  groups  to  have  been  derived  from  those  of  the  Bryo- 
phytes. In  searching  for  the  origin  of  the  leafy  sporophyte,  therefore, 
attention  has  been  focused  upon  the  sporogonia  of  Bryophytes.  .  .  . 
The  doctrine  that  any  plant  structure,  however  important,  can  have 
but  one  phylogeny,  is  hardly  tenable  at  present.  ...  In  contrasting 
the  sporophytes  of  Bryophytes  and  Pteridophytes,  they  seem  to  have 
nothing  in  common  except  that  they  are  usually  derived  from  the 
oospore  and  represent  an  asexual  generation.  These  facts  are  im- 
portant, but  so  are  the  numerous  other  facts  in  which  they  differ 
sharply.  .  .  . 

It  may  be  well  to  contrast  the  leafless  and  leafy  sporophytes.  In 
the  former  case  the  structure  is  never  independent  of  the  gametophyte, 
develops  no  lateral  members,  has  nothing  comparable  to  sporangia, 
and  its  whole  tendency  is  to  render  complex  the  spore-producing 
region.  In  the  latter  case  the  sporophyte  is  dependent  upon  the  game- 
tophyte  only  in  its  embryonic  stage,  develops  prominent  lateral  mem- 
bers, has  distinct  simple  sporangia,  and  its  whole  tendency  is  to  render 
complex  the  sterile  or  nutritive  tissues.  As  one  traces  the  evolution 
of  the  Bryophyte  sporogonia  they  give  evidence  of  increasing  com- 
plexity and  hence  rigidity,  and  little  promise  of  originating  such  a 
diverse  tendency  as  that  shown  by  the  sporophyte  of  Pteridophytes. 
.  .  .  The  origin  of  leaves  on  the  gametophore  of  mosses  suggests  that 
leaves  may  develop  in  response  to  more  favorable  conditions  for  their 
work,  and  such  development  may  result  in  the  great  reduction  of 
chlorophyll  work  done  by  the  less  favored  region,  and  its  consequent 
simplification.  It  is  evident  that  with  the  exchange  of  an  aquatic  for 
a  terrestrial  habit  the  thallose  body  would  not  be  a  favorable  type  for 
chlorophyll  work,  and  that  the  development  of  chlorophyll  tissue  upon 
erect  structures  of  various  kinds  might  follow.  Among  Bryophytes 
the  erect  structure  laid  hold  of  is  the  gametophore,  and  not  the  sporo- 
gonium.  .  .  . 

In  considering  whether  it  is  possible  to  disregard  the  Bryophytes 
in  our  search  for  the  origin  of  the  leafy  sporophyte,  we  are  largely 
influenced  by  the  fact  that  the  Bryophyte  sporophyte,  throughout  its 
whole  history,  is  dominated  by  a  tendency  which  does  not  appear  in 
the  Pteridophyte  sporophyte.  Before  the  establishment  of  alternate 
generations  the  plant  body  may  be  said  to  have  had  three  functions, 
namely,  chlorophyll  work,  and  the  production  of  gametes  and  spores. 
The  appearance  of  the  Bryophyte  sporogonium  was  dominated  by  the 
separation  of  spore-formation  from  the  other  functions,  chlorophyll 
work  being  retained  by  the  garnetophyte,  along  with  gamete-produc- 


PHYLOGEXY  OF  AXGIOSPERMS  291 

tion.  Attention  has  been  focused  so  long  upon  the  gametes  and  spores 
as  the  two  dominant  factors  in  differentiation  that  it  is  hard  to  con- 
ceive of  the  possibility  of  the  domination  of  another  factor.  It  is 
entirely  conceivable,  however,  that  another  form  of  differentiation 
may  have  occurred,  dominated  by  the  needs  of  the  chlorophyll  work, 
and  not  by  spore-production.  Certainly  a  great  need  for  change,  when 
aquatic  conditions  were  exchanged  for  terrestrial,  was  in  connection 
with  the  display  of  chlorophyll  tissue.  It  would  seem  as  if  the  Bryo- 
phytes  had  laid  emphasis  upon  spore-production,  and  therefore  never 
became  organized  for  the  fullest  use  of  terrestrial  conditions,  while  the 
Pteridophytes  laid  emphasis  upon  chlorophyll  work  and  became  highly 
organized  for  terrestrial  life.  It  would  seem  possible,  therefore,  with 
the  three  factors  to  take  into  account,  that  two  distinct  asexual  lines 
may  have  been  organized,  distinct  in  the  factor  selected  to  domi- 
nate. .  .  . 

If  more  favorable  structures  can  be  developed  in  response  to  the 
needs  of  spores  or  gametes,  there  seems  to  be  no  good  reason  why  more 
favorable  structures  may  not  be  developed  in  response  to  the  needs  of 
chlorophyll  work.  If  such  a  response  in  structure  is  possible,  it  would 
naturally  express  itself  first  in  developing  the  largest  display  of  chlo- 
rophyll tissue  in  the  most  favorable  region  of  the  body,  which  would 
gradually  become  differentiated  more  and  more  distinctly  from  the 
rest  of  the  body.  It  does  not  seem  clear  why  the  appearance  of  an 
erect  leafy  axis,  bearing  neither  gametes  nor  spores,  is  not  quite  as 
supposable  as  the  appearance  of  a  sporophore  with  neither  gametes  nor 
leaves,  or  a  gametophore  with  neither  spores  nor  leaves.  .  .  . 

With  such  an  origin  of  the  leafy  sporophyte,  it  would  follow  that 
foliage  leaves  are  not  secondary  but  primary  structures,  and  that  sporo- 
phylls  have  arisen  from  the  differentiation  of  foliage  leaves  bearing 
sporangia,  a  state  of  things  certainly  suggested  by  the  most  primitive 
Pteridophytes  known.  It  would  further  follow  that  the  evolution  of 
the  strobilus  has  followed  the  development  of  foliage  leaves,  a  view  in 
accordance  with  the  older  morphology.  Such  a  view  would  make 
intelligible  the  great  "  gap  "  recognized  as  existing  between  Bryophytes 
and  Pteridophytes,  as  the  two  groups  would  not  be  phylogenetically 
connected,  and  would  have  developed  along  very  divergent  lines  from 
the  first.  It  would  mean  that  at  least  two  independent  sporophyte 
lines  have  appeared,  the  Bryophyte  line  probably  with  an  antithetic 
origin,  and  the  Pteridophyte  line  possibly  with  an  homologous  origin. 
The  great  prominence  of  the  latter  line,  with  its  Spermatophyte 
sequence,  is  correlated  with  the  development  of  a  vascular  system,  and 
it  would  seem  as  though  the  evolution  of  an  elaborate  vascular  system 
must  have  depended  upon  the  domination  of  chlorophyll  work. 

Knowledge  of  the  various  theories  as  to  the  origin  of  species 
is  so  much  a  part  of  the  essential  training  of  the  morphologist 


292  MORPHOLOGY  OP  ANGIOSPERMS 

that  no  resume  of  the  subject  is  necessary.  Until  very  recently, 
the  various  theories  involve  the  idea  that  a  species  is  produced 
as  the  cumulative  result  of  slight  variations  through  successive 
generations.  In  sharp  contrast  to  this  De  Vries  has  recently 
proposed  what  is  called  the  mutation  theory,  a  brief  statement 
of  which  may  be  of  service.  The  experimental  work  that  fur- 
nishes a  substantial  basis  for  the  theory  was  conducted  with 
Angiosperms,  and  a  special  student  of  the  group  should  be  pre- 
pared to  recognize  any  testimony  for  or  against  it.  A  suggest- 
ive feature  of  the  work  of  De  Vries  is  his  attempt  to  break 
away  from  the  speculative  method  and  to  subject  the  problem 
to  experimental  investigation.  Whether  his  results  indicate  a 
general  method  of  the  origin  of  species  in  nature  or  an  occa- 
sional method,  or  are  capable  of  an  entirely  different  expla- 
nation and  hold  no  relation  to  the  normal  origin  of  species, 
remains  for  future  work  to  determine.  In  any  event,  the  theory 
will  stimulate  investigation  and  deserves  consideration. 

The  occasional  sudden  appearance  of  what  have  been  called 
"  sports  "  is  well  known,  but  they  have  not  been  prominently 
associated  with  the  origin  of  species.  They  have  been  referred 
to  as  cases  of  "  saltatory  evolution,"  and  in  1864  Kolliker 
seems  to  have  been  responsible  for  the  term  "  heterogenesis  " 
as  applied  to  this  phenomenon.  Quite  independently  and  sim- 
ultaneously De  Vries  11  and  Korschinsky  12  have  elaborated  the 
same  theory  as  to  the  origin  of  species,  the  former  calling  it 
the  "  mutation  theory,"  the  latter  using  Kb'lliker's  name  "  hete- 
rogenesis." Korschinsky  has  brought  together  a  mass  of  data 
from  the  records  of  gardeners  and  horticulturists  to  show  that 
most  of  the  culture  "  varieties  "  have  arisen  through  heterogene- 
sis rather  than  by  selection.  De  Vries,  on  the  other  hand,  has 
experimented  extensively  with  CEnothera  Lamarckiana,  a  spe- 
cies showing  mutability  in  a  high  degree.  This  American  spe- 
cies was  found  naturalized  on  an  area  in  Holland  about  1875, 
and  afterward  spread  rapidly.  When  observed  by  De  Vries, 
in  1886,  two  new  species  were  detected  among  the  normal  forms, 
and  they  have  maintained  themselves  ever  since.  From  1886 
until  the  publication  of  his  book,  De  Vries  made  observations 
upon  the  naturalized  areas  and  carried  on  cultures  in  the  botan- 
ical garden  at  Amsterdam.  As  a  general  result,  it  may  be  stated 
that  out  of  50,000  seedlings  of  (E.  Lamarckiana  800  were  nm- 


PHYLOGENY  OF  AXGIOSPERMS  293 

tants.  Of  these  800,  about  200  were  the  new  species  named 
(E.  lata ;  that  is,  the  same  new  species  appeared  about  200 
times.  Various  other  new  species  appeared,  and  were  preserved 
by  culture.  The  mutants  also  occurred  in  every  direction  in 
the  same  environment,  showing  no  indication  of  being  responses 
to  external  conditions.  In  the  great  majority  of  cases  the  mu- 
tants were  constant  from  the  outset,  there  being  no  development 
and  fixation  of  characters  through  selection,  and  no  transition 
between  parent  and  offspring.  Experiments  with  other  species 
seem  to  indicate  that  the  majority  of  species  are  at  present 
immutable,  varying  writhin  certain  narrow  limits,  but  not  giving 
rise  to  mutants. 

Solms-Laubach 10  has  shown  that  in  all  probability  Cap- 
sella  Heegeri  has  arisen  in  this  way  from  C.  Bursa-pastoris ; 
and  Carlson  13  has  suggested  a  similar  origin  for  certain  Swed- 
ish forms  of  Succisa  pratensis ;  while  Jordan's  work  with  Draba 
verna  has  discovered  about  200  immutable  forms  within  the 
old  species  limits,  that  probably  represent  true  species  derived 
by  mutation  from  a  parent  of  great  mutability. 

The  experiments  of  De  Vries  seem  to  indicate  that  there  is 
a  definite  limit  to  individual  variability,  beyond  which  selection 
can  not  go.  Furthermore,  it  is  claimed  that  selection  never  fixes 
a  character,  but  reversion  may  occur  after  any  number  of  gen- 
erations of  culture.  In  short,  natural  selection  can  not  create 
anything  new,  but  can  modify  within  definite  and  narrow  lim- 
its ;  while  mutation  brings  into  existence  something  new,  which 
will  continue  as  a  new  species  if  it  can  survive  the  struggle  for 
existence.  There  is  thus  drawn  a  sharp  contrast  between  muta- 
bility and  ordinary  variability,  the  latter  being  governed  by 
environment,  the  former  independent  of  it.  Hence,  while  most 
species  are  immutable,  all  are  more  or  less  variable. 

At  its  present  stage  such  a  theory  can  not  be  accepted  or 
rejected.  Either  alternative  will  demand  a  vast  amount  of  care- 
fully sifted  experimental  evidence.  It  should  be  remembered 
that  the  subject  lends  itself  readily  to  observations  that  are 
really  inferences,  and  a  vast  amount  of  data  will  doubtless  be 
forthcoming  that  can  not  be  regarded  as  testimony.  The  stu- 
dent of  Angiosperms,  however,  is  in  a  position  to  encounter 
useful  data,  for  the  group  is  a  very  modern  one  and  seems  to 
contain  many  mutable  species.  It  should  further  be  remem- 


294:  MORPHOLOGY  OF  ANG10SPERMS 

bered  that  the  whole  theory  is  based  upon  the  present  concep- 
tion of  species,  a  conception  so  variable  that  it  can  not  be 
defined.  Furthermore,  although  there  may  be  a  fixed  limit 
to  ordinary  variation,  there  must  also  be  a  fixed  limit  to  the 
extraordinary  variation  called  mutation,  and  this  remains  to  be 
defined.  In  fact,  there  is  evidence  that  extreme  mutation  re- 
sults in  functional  derangement  of  organs,  and  the  result  is  a 
monstrosity,  which  may  be  regarded  as  an  impossible  new  spe- 
cies. Finally,  even  if  mutation  be  found  to  explain  the  origin 
of  many  new  species,  it  does  not  follow  that  other  processes 
also  may  not  be  working  to  the  same  result. 

In  a  recent  paper,  Strasburger  19  takes  occasion  to  discuss 
the  origin  of  species,  taking  the  view  that  the  results  of  natural 
selection  have  been  overestimated,  and  that  new  species  have 
arisen  through  mutation,  due  to  internal  causes  alone,  and 
through  "  use  and  disuse/'  by  means  of  which  a  certain  amount 
of  adaptation  to  environment  is  secured.  To  him  the  only  func- 
tion of  natural  selection  appears  to  be  to  remove  the  less  valu- 
able forms  produced  through  mutation  and  "  use  and  disuse." 
It  follows  that  the  ordinary  physiological  operations  do  not 
result  in  species,  but  affect  them  after  they  have  appeared,  and 
that  the  origin  of  species  is  a  morphological  rather  than  a  phys- 
iological problem. 

LITERATURE  CITED 

1.  BOWER,  F.  O.    A  Theory  of  the  Strobilus  in  Archegoniate  Plants. 

Annals  of  Botany  8 :  343-365.  1894. 

2.  DELPIXO,  F.     Applicazione  de  nuovi  criterii  per  la  classificasione 

delle  piante.     Mem.  Real.  Accad.  Sci.   Bologna  V.    6:    83-116. 
1896  ;  see  review  Bot.  Centralbl.  67  :  370.  1896. 

3.  BESSEY,  C.  E.     Phylogeny  and  Taxonomy  of  the  Angiosperms. 

Bot.  Gazette  24:  145-178.  1897. 

4.  KLEBS,  G.    Alternation  of  Generations  in  the  Thallophytes.    Aii- 

nals  of  Botany  12:  570-583.  1898. 

5.  LANG,  W.  H.    Alternation  of  Generations  in  the  Archegoniates. 

Annals  of  Botany  12:  583-592.  1898. 

6.  HARTOG,  M.    Alternation  of  Generations.     Annals  of  Botany  12 : 

593-594.  1898. 

7.  HOLM,  THEO.     Podophyllum  peltatum ;  a  Morphological  Study. 

Bot.  Gazette  27 :  419-433.  figs.  10.  1898. 

8.  COULTER,   J.   M.     The    Origin  of    the   Leafy  Sporophyte.     Bot. 

Gazette  28:  46-59.  1899. 


PHYLOGENY  OF  ANGIOSPERMS  295 

9.  QUEVA,  C.    Contributions  a  Tanatomie  des  Monocotyledonees.  I. 
Les  Uvulariees  tubereuses.     Lille.  1899. 

10.  SOLMS-LAUBACH,   H.      Cruciferenstudien.    1.      Capsella   Heegeri 

Solms,  eine  neue  entstandene  Form  der  deutschen  Flora.  Bot. 
Zeit.  58i :  167-190.  pi.  7.  1900. 

11.  DE  TRIES,  H.    Die  Mutationstheorie,  Versuche  und  Beobachtungen 

iiber  die  Entstehung  von  Arten  im  Pflanzenreich.  Vol.  I.  Leip- 
zig. 1901.  See  reviews:  Biol.  Centralbl.  21:  257-269,  289-305. 
1901 ;  Bot.  Centralbl.  87 :  170.  1901 ;  Bot.  Gazette  33 :  236.  1902. 
Also  The  Origin  of  Species  by  Mutation,  Science  15 :  721-729. 
1902. 

12.  KORSCHIXSKY,  S.     Heterogenesis  und  Evolution.    Ein  Beitrag  zur 

Theorie  der  Entstehung  der  Arten.  Translated  from  the  Russian 
by  S.  Tschulok.  Flora  89:  240-363.  1901;  also  review  in  Bot. 
Gazette  33:  396.  1902. 

13.  CARLSON,  G.  \V.  F.     Ett  par  afvikande  former  af  Succisa  praten- 

sis.     Bot.  Notiser  1901 :  224-226. 

14.  LYOX,  H.  L.    Observations  on  the  Embryogeny  of  Nelumbo.    Minn. 

Bot.  Studies  2 :  643-655.  1901. 

15.  CAMPBELL,  D.  H.     On  the  Affinities  of  Certain  Anomalous  Dicot- 

yledons.   Amer.  Nat.  36:  7-12.  1902. 

16.  KARSTEX,  G.     Ueber  die  Entwickelung  der  weiblichen  Bliithen 

bei  einigen  Juglandaceen.     Flora  90:  316-333.  pi  12.  1902. 

17.  LYOX,  H.  L.    The  Phylogeny  of  the  Cotyledon.     Postelsia  1901 : 

55-86.  1902. 

18.  SARGAXT,  ETHEL.    The  Origin  of  the  Seed-leaf  in  Monocotyledons. 

New  Phytologist  1 :  107-113.  pi.  2.  1902. 

19.  STRASBURGER,  E.     Ein  Beitrag  zur  Kenntniss  von  Ceratophyllum 

submersum  und  phylogenetische  Erorterungen.  Jahrb.  Wiss. 
Bot.  37:  477-526.  pis.  9-11.  1902. 

20.  HALLIER,  H.     Beitrage  zur  Morphologic  der  Sporophylle  und  des 

Trophophylls  in  Beziehung  zur  Phylogenie  der  Kormophyten. 
Jahrb.  Hamburgischeii  Wiss.  Anstalten  19:  1-110.  1902. 

21.  SARGAXT,  ETHEL.     A  Theory  of  the  Origin  of  Monocotyledons, 

founded  on  the  Structure  of  their  Seedlings.  Annals  of  Botany 
17:  1-92.  pis.  1-7.  1903. 


20 


CHAPTEK    XVI 

COMPABATIVE   ANATOMY   OF   THE   GYMNOSPERMS   AND 
THEIR   ALLIES  * 

THE  skeletal  structure  of  vascular  plants  has  in  the  past 
been  used  for  phylogenetic  purposes  to  a  much  smaller  extent 
than  that  of  the  higher  animals.  During  recent  years,  however, 
important  advances  in  our  knowledge  of  the  anatomy  of  fossil 
plants  have  made  it  apparent  that  the  primary  fibrovascular 
skeleton  of  the  vascular  plants  is  even  more  conservative  than 
their  reproductive  organs,  and  consequently  of  great  impor- 
tance in  arriving  at  the  relationships  of  the  larger  groups.  The 
most  extreme  ecological  conditions,  acting  for  long  periods,  seem 
to  have  little  effect  in  modifying  the  essential  features  of  the 
primary  fibrovascular  framework,  so  that,  for  example,  the 
extremely  xerophytic  cactus  and  the  hydrophytic  water-lily 
have  exactly  the  same  type  of  skeleton  from  the  standpoint  of 
comparative  anatomy.  It  sometimes  happens,  however,  that 
the  woody  framework  is  extremely  complex  in  the  adult.  Re- 
cent investigations  which  cover  the  whole  field  of  living  vascular 
plants  make  it  clear  that  the  study  of  the  development  of  the 
sporeling  or  seedling  provides  a  satisfactory  key  to  the  inter- 
pretation of  the  most  intricate  skeletal  structures  of  maturity. 

A  brief  account  of  certain  general  results  of  recent  anatom- 
ical and  developmental  research  in  the  case  of  the  vascular 
plants  is  accordingly  necessary  for  an  understanding  of  those 
skeletal  features  of  the  Gymnosperms  and  their  allies  which 
are  of  phylogenetic  importance. 

PTEEIDOPHYTES 

The  simplest  type  of  stem  in  the  Pteridophytes  is  that  in 
which  there  is  present  a  single  pithless  fibrovascular  conductive 

*  Contributed  by  Professor  Edward  C.  Jeffrey,  of  Harvard  University. 
296 


COMPARATIVE  ANATOMY  OF  GYMNOSPERMS  297 

strand  embedded  in  the  parenchyma  of  the  fundamental  tissue. 
Part  of  a  transverse  section  of  such  a  stem  is  seen  in  Fig.  108,  A. 
In  the  center  is  the  concentric  fibrovascular  bundle  or  stele, 
which  consists  of  a  mass  of  xylem  completely  surrounded  by 
phloem.  The  stele  or  central  cylinder  is  bounded  in  turn  by 
brown  sclerenchymatous  fundamental  tissue.  This  type  of 
stem,  since  it  is  a  very  primitive  one,  may  conveniently  be 
called  "  protostelic  "  (Jeffrey19). 

Another  common  condition  of  the  stem  is  seen  in  Fig.  108, 
J9,  which  represents  a  cross-section  of  the  rhizome  of  Adiantum 
pedatum.  In  this  case  the  central  cylinder  is  not  a  solid  fibro- 
vascular strand  as  in  the  preceding  example,  but  a  hollow  cyl- 
inder filled  with  fundamental  tissue  like  that  external  to  the 
stele.  The  plane  of  section  is  just  above  the  point  of  origin  of 
a  leaf-trace,  which  may  be  distinguished  as  the  smaller  of  the 
two  concentric  masses  of  fibrovascular  tissue.  At  a  higher  level 
the  gap  in  the  cauline  central  cylinder  closes,  and  the  stele  be- 
comes circular  instead  of  crescentic  in  cross-section.  Similar 
gaps  appear  above  all  the  outgoing  leaf-traces,  and  as  a  conse- 
quence the  central  cylinder  is  essentially  a  concentric  fibrovas- 
cular tube,  with  gaps  in  its  walls  corresponding  to  the  leaf- 
traces.  The  type  of  central  cylinder  which  has  just  been  de- 
scribed may  appropriately  be  termed  "  siphonostelic "  (Jef- 
frey19). 

Fig.  108,  C,  is  from  a  photograph  of  the  adult  stem  of 
Pteris  aquilina,  the  common  bracken  fern.  In  this  case  there 
are  numerous  concentric  fibrovascular  bundles  present  in  the 
fundamental  tissue  of  the  rhizome,  and  accordingly  stems  of 
this  type  have  been  designated  by  Van  Tieghem  "  polystelic." 
It  has  been  shown,  however,  that  in  such  stems  as  are  exempli- 
fied by  P.  aquilina  the  primitive  condition  of  the  central  cyl- 
inder is  a  stelar  tube  with  foliar  lacunae  (Jeffrey19).  Fig. 
108,  D,  from  the  young  stem  of  P.  aquilina :,  sufficiently  demon- 
strates the  truth  of  this  statement.  The  young  stem  gradually 
passes  into  the  condition  represented  in  Fig.  108,  (7,  first  by 
the  foliar  gaps  becoming  so  long  as  to  overlap,  and  second  by 
the  derivation  of  the  large  central  strands  from  the  inner  wall 
of  the  primitive  stelar  tube.  Consequently  the  stem  of  P.  aqui- 
lina may  be  regarded  on  ontogenetic  grounds  as  siphonostelic 
and  essentially  similar  to  that  of  Adiantum  pedatum. 


298  MORPHOLOGY  OF  ANGIOSPERMS 

Fig.  108,  Ej  shows  a  type  of  central  cylinder  which  at  first 
sight  appears  very  like  that  of  the  adult  stem  of  Pteris  aqui- 
lina]  above  on  the  right  is  a  gap  in  the  tubular  stele,  which 
in  this  case  corresponds  to  a  branch.  Laterally,  on  the  left, 
a  foliar  trace  is  to  be  seen  in  the  fundamental  tissue.  The  leaf- 
trace  is  very  small,  and  there  is  no  gap  in  the  central  cylinder 
corresponding  to  it.  As  in  P.  aquilina,  there  are  two  medullary 
fibrovascular  strands.  It  has  recently  been  shown  (Jeffrey  13' 10) 
that  in  certain  great  groups  of  plants  foliar  gaps  are  constantly 
present,  while  in  other  great  groups  they  are  unfailingly  ab- 
sent. The  type  of  tubular  stele  characterized  by  the  presence 
of  foliar  gaps  has  been  called  "  phyllosiphonic,"  and  that  pos- 
sessing only  gaps  for  the  branches  or  ramular  lacunae  "  clado- 
siphonic."  These  distinctions  are  extremely  constant,  and  con- 
sequently of  great  phylogenetic  value. 

Fig.  108,  F,  is  from  a  photograph  of  a  cross-section  of  the 
central  cylinder  of  Osmunda  Claytoniana.  It  is  of  special  in- 
terest because  it  is  obviously  of  the  same  type  as  the  central 
cylinder  of  the  living  Gymnosperms,  viz.,  a  ring  of  collateral 
bundles  surrounding  a  medulla  and  separated  from  each  other 
by  medullary  rays.  Van  Tieghem  4  regards  this  type  of  stele 
as  derived  by  dilatation  from  the  prostostelic  condition,  with 
the  formation  of  pith  and  medullary  rays  from  the  stelar  pa- 
renchyma. According  to  this  view,  the  pith  and  rays  are  mor- 
phologically different  from  and  have  nothing  in  common  with 
the  fundamental  tissue  surrounding  the  stele. 

Fig.  109,  6r,  shows  the  forking  of  the  central  cylinder  of 
Osmunda  cinnamomea.  In  this  example  the  pith  is  obviously 
continuous  with  the  external  cortex,  and  a  strand  of  the  very 
characteristic  brown  sclerenchymatous  tissue  of  the  cortex  is 
passing  down  into  the  medullary  parenchyma  through  the  gap 
between  the  divisions  of  the  fork.  It  is  to  be  noted  further 
that  the  phloem  passes  inward  around  the  divisions  of  the  fork 
for  a  considerable  distance,  and  the  endodermis  is  as  well 
marked  on  the  inside  as  on  the  outside  of  the  crescentic  zones 
of  bundles.  In  Fig.  109,  H,  there  appears  a  not  unusual  con- 
dition of  the  central  cylinder  in  0.  cinnamomea.  Unlike  0. 
Claytoniana,  there  is  present  an  internal  endodermis  along  the 
inner  margin  of  the  bundles,  and  the  medulla  is  often  charac- 
terized by  the  presence  of  a  mass  of  brown  sclerenchyma  similar 


COMPARATIVE  ANATOMY  OF  GYMNOSPERMS  299 

to  that  which  constitutes  the  external  portion  of  the  funda- 
mental tissue  of  the  stem. 

Fig.  109,  I,  shows  a  central  cylinder  of  Osmunda  cinna- 
momea,  where  not  only  an  internal  endodermis  is  present  but 
also  internal  phloem  as  well.  In  Fig.  109,  J,  a  part  of  the 
wall  of  the  same  central  cylinder  is  shown  more  highly  mag- 
nified. The  sieve-tubes  are  easily  recognized  as  large,  appar- 
ently empty  elements.  It  has  been  suggested  by  Jeffrey  19  and 
Faull,18  as  a  result  of  the  study  of  the  anatomy  of  the  whole 
order,  that  the  type  of  central  cylinder  found  in  the  Osmunda- 
ceae  is  the  result  of  reduction  from  a  siphonostelic  condition 
with  internal  phloem.  This  view  of  the  matter  is  strengthened 
by  the  fact  that  brown  sclerenchyma  is  sometimes  found  in  the 
pith  of  Osmunda  regalis  and  Todea  barbara,  although  in  these 
species  there  is  no  longer  any  communication  between  pith  and 
cortex  in  the  region  of  forking.  Moreover,  exactly  similar 
series  of  degeneration  to  that  supplied  by  the  Osmundaceae 
have  been  shown  to  exist  in  the  case  of  certain  polypodiaceous 
ferns.  Hence  it  may  be  assumed,  in  the  present  connection, 
that  the  type  of  central  cylinder  exemplified  by  the  Osmunda- 
ceae has  arisen  by  degeneracy  from  the  siphonostelic  type  with 
internal  phloem ;  and  that  the  medulla  often  shows  signs  of  its 
origin  by  striking  histological  resemblance  to  the  cortex,  even 
when  there  is  no  longer  any  communication  between  the  med- 
ullary and  cortical  fundamental  tissues. 

Fig.  109,  K,  shows  the  structure  of  one  of  the  tracheary 
strands  of  Osmunda  cinnamomea.  The  protoxylem  or  primi- 
tive wood  appears  as  a  cluster  of  small  elements,  just  external 
to  a  mass  of  wood-parenchyma.  The  protoxylem  does  not  abut 
immediately  on  the  pith,  as  in  the  seed-plants,  but  is  separated 
from  it  by  a  considerable  amount  of  wood-parenchyma  and  me- 
taxylem ;  most  of  the  metaxylem,  however,  lies  external  to  the 
protoxylem.  This  type  of  tracheary  bundle  is  very  character- 
istic of  the  ferns,  and  has  been  designated  "  mesarch." 

In  the  case  of  the  Lycopodiales,  the  tracheary  bundle  is  of 
still  another  type.  If  Fig.  108,  E,  be  examined,  it  will  be  seen 
that  on  the  left  of  the  central  cylinder,  opposite  the  leaf-trace 
in  the  cortex,  is  a  cluster  of  protoxylem.  The  primitive  wood 
in  this  case  is  external  and  next  the  phloem.  This  feature  is 
very  characteristic  of  the  Lycopods  and  their  allies.  Bundles 


300  MORPHOLOGY  OF  ANGIOSPERMS 

of  the  type  j  list  mentioned  have  been  designated  by  Scott  6 
"  exarch.77  Hence  it  may  be  stated  that  the  bundles  of  the  Fern- 
like  plants  are  characteristically  mesarch;  that  the  Lycopods 
and  their  allies  have  exarch  bundles;  and  that  the  prevailing 
type  in  the  Spermatophytes  is  the  endarch  bundle,  the  primitive 
wood  here  coming  next  the  medulla.  These  anatomical  distinc- 
tions, however,  are  less  trustworthy  than  those  depending  on 
the  presence  and  absence  of  foliar  gaps,  for  many  Ferns  have 
endarch  bundles,  while  some  (Lygodium,  etc.)  have  even  exarch 
tracheary  strands;  on  the  other  hand,  Phylloglossum,  a  recog- 
nized Lycopod,  has  distinctly  mesarch  cauline  bundles.  There 
are  no  known  examples,  however,  of  siphonostelic  Lycopods 
(Jeffrey10)  with  foliar  gaps,  or  of  siphonostelic  Ferns  without 
them. 

CYCADOFILICES 

Recently  Potonie  n  has  established  a  group,  the  Cycado- 
filices,  to  include  a  number  of  fossil  forms  which  are  neither 
true  Ferns  nor  typical  Gymnosperms,  but  which  possess  to  a 
large  degree  anatomical  features  of  both  alliances.  These  forms 
can  now  be  more  advantageously  discussed  after  the  general 
anatomical  account  presented  in  the  foregoing  paragraphs.  The 
vegetative  anatomy  of  the  Cycadofilices  is  of  special  importance, 
both  because  of  our  entire  ignorance  of  their  reproductive  or- 
gans at  the  present  time  and  because  their  anatomical  structure 
presents  such  an  interesting  transition  from  the  pteridophytic 
to  the  gymnospermous  type. 

Heterangium. — Fig.  109,  L,  taken  from  Scott's  admirable 
Studies  in  Fossil  Botany,  shows  the  structural  features  of  the 
stem  of  Heterangium  Grievii,  a  primitive  representative  of  the 
Cycadofilices.  The  central  cylinder  is  obviously  protostelic  and 
very  similar  to  that  of  Gleichenia  flabellata  of  Fig.  108,  A. 
A  striking  difference,  however,  is  the  presence,  on  the  outside 
of  the  pithless  primary  wood,  of  a  narrow  zone  of  secondary 
wood  which  is  clearly  distinguishable  by  reason  of  the  regular 
radial  arrangement  of  its  elements.  In  the  cortex  may  be  seen 
leaf-traces  and  groups  of  sclerotic  cells.  The  external  cortex 
is  bounded  by  a  very  characteristic  hypodermal  zone,  which  in 
transverse  section  appears  to  be  made  up  of  alternating  stripes 
of  parenchymatous  and  sclerenchymatous  cells.  Viewed  longi- 


COMPARATIVE  ANATOMY  OF  GYMXOSPERMS  301 

tudinally,  the  hypoderma  is  seen  to  be  composed  of  a  tangential 
network  of  sclerenchymatous  fibers  having  the  meshes  filled 
with  parenchyma. 

Medullosa. — Fig.  110,  M,  reproduces  a  diagrammatic  trans- 
verse section  of  the  stem  of  Medullosa  anglica.  On  the  outside 
of  the  stem  can  be  distinguished  the  same  curious  hypoderma 
which  is  characteristic  of  the  genus  briefly  described  above. 
The  central  cylinder  in  this  case,  however,  is  obviously  not  pro- 
tostelic,  but  polystelic.  Each  of  the  large  fibrovascular  strands 
is  characterized  by  the  presence  of  a  considerable  zone  of  sec- 
ondary wood,  which  is  indicated  in  the  diagram  by  radiating 
lines.  There  are  no  sclerifications  in  the  cortex ;  but  numerous 
mucilage  ducts,  similar  to  those  of  the  Marattiaceae  and  the 
Cycads,  may  be  seen  in  the  fundamental  tissue,  both  outside  and 
between  the  large  fibrovascular  strands,  although  their  occur- 
rence in  the  latter  position  is  not  shown  in  the  diagram. 

Very  often  the  arrangement  of  the  bundles  in  species  of 
Medullosa  was  much  more  complex  than  that  appearing  in  Fig. 
110,  M.  It  has  been  shown  recently  that  in  ferns  with  even 
the  most  complex  arrangement  of  the  bundles  in  the  adult,  by 
following  the  development  it  is  possible  to  arrive  at  the  simple 
stelar  tube  as  a  starting-point  (Jeffrey19).  It  is  consequently 
-extremely  probable  that  the  bundle  system  of  the  Medullosae  is 
to  be  regarded  as  primitively  siphonostelic,  like  that  of  Pteris 
aquilina. 

In  Fig.  110,  N,  is  represented  a  cross-section  of  a  part  of 
the  stem  of  Medullosa  Solmsi.  Here  are  to  be  seen  numerous 
bundles,  some  of  which  are  broad  and  plate-like  and  others 
small  and  rounded  in  outline.  The  broader  bundles  are  known 
as  "  plate-rings,"  and  the  smaller  ones  as  "  star-rings."  An 
interesting  feature  of  the  outer  plate-rings  is  the  fact  that  the 
zone  of  secondary  wood  on  the  external  face  of  the  bundles  is 
often  very  much  thicker  than  that  on  the  internal  face.  This 
peculiarity  is  especially  well  marked  in  old  stems  of  M.  stellata. 

Luginodendron. — Fig.  110,  0,  taken  from  Williamson  and 
Scott,6  reproduces  admirably  the  general  features  of  structure 
of  the  stem  Lyginodendron  Oldhamium.  On  the  outside  is 
the  same  curious  hypoderma]  layer  which  occurs  in  Heteran- 
yium  and  Medullosa.  There  is  present  also  a  zone  of  periderm 
external  to  the  fibrovascular  tissues.  In  the  cortex  may  be  seen 


302  MORPHOLOGY  OF  ANGIOSPERMS 

clusters  of  sclerenchymatous  tissue.  These  are  also  found  in 
the  foliar  gaps  and  in  the  pith.  In  the  case  of  Lyginodendron 
the  primary  wood  is  comparatively  poorly  developed  and  occurs- 
as  distinct  islands  along  the  margin  of  the  medulla.  The  sec- 
ondary wood  is  characterized  by  the  regular  radial  seriation  of 
its  elements  and  is  abundant,  but,  in  common  with  many  other 
fossil  Pteridophytes  with  secondary  growth,  shows  no  indica- 
tion of  annual  rings.  The  continuity  of  the  woody  zone  is 
completely  interrupted  at  intervals  by  the  foliar  gaps  which 
subtend  the  outgoing  leaf-traces. 

Fig.  110,  P,  is.  a  photograph  of  part  of  the  ligneous  zone 
of  L.  Oldhamium.  The  protoxylem,  distinguished  by  the  small 
size  of  its  elements,  is  seen  to  be  embedded  in  the  primary  wood. 
Most  of  the  primary  metaxylem  lies  on  the  medullary  side  of 
the  protoxylem,  and  a  smaller  portion  between  it  and  the  sec- 
ondary wood.  Hence  the  primary  bundle  is  mesarch,  as  is  often 
the  case  in  the  Ferns  and  their  allies.  Another  important  fili- 
cinean  feature  is  the  presence  of  well-marked  foliar  gaps. 

Fig.  110,  Q,  taken  from  Williamson  and  Scott,6  shows  an 
interesting  departure  from  the  usual  state  of  affairs  in  L.  Old- 
hamium', a  primary  wood-bundle  is  present,  and  external  to  it 
is  the  usual  secondary  wood.  In  this  case,  however,  there  is 
secondary  wood  and  phloem  on  the  medullary  side  of  the  bundle 
as  well.  The  condition  represented  in  the  figure  is  quite  un- 
usual in  L.  Oldhamium ;  but,  as  has  been  shown  by  Seward,  is 
of  common  occurrence  in  L.  robustum.  The  facts  just  described 
are  of  particular  interest,  because  Scott  6  has  made  a  specific 
comparison  between  the  central  cylinders  of  Lyginodendron  and 
Osmunda ;  and  indeed,  if  we  imagine  a  secondary  zone  of  wood 
present  in  the  latter  genus  and  the  primary  wood-bundles  cor- 
respondingly reduced  in  size,  the  resemblance  becomes  very 
close.  The  occurrence  of  internal  phloem  and  secondary  wood 
is  paralleled  by  the  discovery  of  internal  phloem  in  0.  cinna- 
momea. 

The  forms  described  above  sufficiently  illustrate  the  variety 
of  structure  in  the  stem  of  the  Cycadofilices,  and  it  now  be- 
comes necessary  to  discuss  their  phylogenetic  significance.  First 
of  all  is  to  be  noted  the  fact  that  they  represent  the  three  types 
of  stelar  structure  described  at  the  beginning  of  the  chapter : 
Heterangium  being  protostelic  like  Gleichenia ;  Medullosa  sipho- 


COMPARATIVE  ANATOMY  OF  GYMNOSPERMS  303 

nostelic  like  Adiantum  pedatum  and  Pteris  aqutiina]  and  Lygi- 
nodendron  siphonostelic,  without  internal  phloem,  as  is  gener- 
ally the  case  in  Osmunda,  but  resembling  this  genus  in  the  occa- 
sional occurrence  of  internal  sieve-tissue.  The  only  striking 
anatomical  difference  between  the  cycadofilicinean  forms  de- 
scribed above  and  the  parallel  cases  from  the  ferns  lies  in  the 
absence  of  secondary  growth  in  the  latter.  This  feature  is  now 
known  to  be  of  minor  importance,  although  great  weight  was- 
attached  to  it  by  the  Brongniartian  school  of  paleobotanists. 

In  regard  to  the  particular  type  of  the  Cycadofilices  which 
gave  rise  to  the  Gymnosperms  there  is  some  difference  of  opin- 
ion. Potonie,9'  n  Worsdell,16' 17  and  Jeffrey 19  consider  the 
Cycads  to  be  derived  from  Medullosa-like  ancestors  through  a 
Lyginodcndron-like  phase,  by  the  gradual  disappearance  of  the 
internal  secondary  wood,  and  the  final  suppression  of  the  cen- 
tripetal primary  wood.  Scott,6' 15  on  the  other  hand,  regards 
Lyyinodendron  as  the  ancestral  type,  and  as  derived  directly 
from  Heterangiuni  by  the  formation  of  an  intrastelar  pith,  and 
not  from  medullosan  ancestors  by  reduction.  He  further  con- 
siders the  Medullosae  to  constitute  merely  a  side  branch  of  the 
phylogenetic  tree,  and  expresses  the  opinion  that  "  we  should 
involve  ourselves  in  unnecessary  complications  if  we  endeav- 
ored to  derive  the  simple  primary  structure  of  the  cycadean 
stem  from  the  more  elaborate  organization  of  a  Medullosa." 
However,  examples  of  phylogenetic  progression  from  the  com- 
plex to  the  simple  are  not  at  all  uncommon.  Striking  illustra- 
tions of  this  principle  are  afforded  by  the  derivation  of  the 
simple  hyoid  bone  of  the  mammals  from  the  complex  hyoid 
apparatus  of  the  lower  vertebrates,  and  the  evolution  of  the 
monodactyl  horses  of  the  present  day  from  their  four-toed  an- 
cestors of  the  Eocene.  The  histological  structure  of  the  medulla 
in  Lyginodendron  strikingly  resembles  that  of  the  cortex  in  the 
presence  of  sclerotic  nests,  and  this  feature  indicates  strongly 
community  of  origin  of  the  medullary  and  cortical  tissues. 
Further,  the  occasional  occurrence  of  internal  phloem  and  in- 
ternal secondary  wood  in  Lyginodendron  can  most  easily  be  ex- 
plained as  a  vestigial  relic  of  a  siphonostelic  condition,  in  which 
internal  phloem  was  normally  present — i.  e.,  a  Medullosa  with 
a  single  series  of  bundles. 

In  regard  to  the  special  pteridophytic  ancestry  of  the  Cyca- 


304  MORPHOLOGY  OF  ANGIOSPERMS 

dofilices  there  now  seems  to  be  little  doubt.  Scott  has  pointed 
out  that  their  fern-like  foliage  and  usually  mesarch  bundles 
indicate  strongly  a  filicinean  as  opposed  to  a  lycopodinean  ori- 
gin. It  has  further  recently  been  shown  that  they  are  phyllo- 
siphonic  (Jeffrey19),  and  since  this  feature  is  quite  exclusively 
characteristic  of  the  ferns,  it  seems  impossible  to  derive  the 
Cycadofilices  from  the  Lycopods,  as  has  been  done  by  Renault.2 

CYCADALES     ' 

The  leaves  and  fern-like  habit  of  the  Cycads  afford  good 
external  evidence  of  their  filicinean  origin,  and  their  multicili- 
ate  sperms  point  in  the  same  direction.  The  strongest  evidence 
of  their  having  come  from  the  ferns,  however,  is  supplied  by 
their  fibrovascular  anatomy. 

Fig.  Ill,  R,  is  from  a  photograph  of  a  cross-section  of  the 
stem  of  Zamia  floridana.  Both  pith  and  cortex  are  occupied, 
as  in  Medullosa,  by  numerous  mucilage  ducts.  In  the  cortex 
several  curved  lines  are  present,  which  represent  the  curved 
course  of  the  foliar  traces  and  are  known  as  "  girdles."  Al- 
though some  years  old,  the  fibrovascular  zone  is  quite  narrow, 
and  shows  no  evidence  of  annual  rings,  a  feature  of  resemblance 
to  the  Medullosae  and  Lyginodendron. 

In  Fig.  Ill,  89  the  central  cylinder  of  the  same  species  is 
shown  more  highly  magnified.  Its  continuity  is  obviously 
broken  by  gaps,  which  subtend  the  outgoing  leaf-traces.  The 
mucilage  ducts  of  the  medulla  join  with  those  of  the  cortex 
through  the  foliar  gaps.  The  central  cylinder  of  Zamia,  which 
is  quite  typical  of  the  Cycads  in  this  respect,  is  consequently 
phyllosiphonic.  The  mucilage  ducts  of  the  Cycads  do  not  pene- 
trate into  the  leaf-traces  or  root-steles.  Hence  it  may  be  as- 
sumed that,  as  in  the  Marattiaceae  and  Medullosae,  they  are 
characteristic  only  of  the  extrastelar  fundamental  tissue.  The 
pith  of  the  Cycads,  which  contains  mucilage  ducts  continuous 
with  those  of  the  cortex,  is  to  be  compared,  therefore,  with  the 
mucilaginous  medulla  of  one  of  the  Marattiaceae  or  of  a  Medul- 
losa, and  is  to  be  regarded  as  extrastelar. 

The  foliar  traces  of  the  Cycads  are  quite  unique  in  struc- 
ture and  of  considerable  phylogenetic  importance.  The  first 
complete  description  of  them  was  given  by  Mettenius.1  As  has 
already  been  pointed  out,  the  course  of  cycadean  leaf-traces  is 


COMPARATIVE  ANATOMY  OF  GYMNOSPERMS  305 

peculiar;  for,  instead  of  passing  directly  from  the  central  cyl- 
inder into  the  leaf,  they  usually  pursue  a  circular  course,  so 
that  they  reach  their  corresponding  leaf  on  the  opposite  side  of 
the  stem  from  their  point  of  origin.  In  Zamia  I  have  observed 
this  arrangement  of  the  traces  even  in  the  seedling;  but  in 
Cycas,  according  to  Mettenius,1  the  leaf-traces  of  the  young 
plant  at  first  pursue  a  direct  course,  although  at  a  later  stage 
girdles  are  present.  During  their  cortical  course  the  foliar 
traces  often  undergo  more  or  less  complex  anastomoses.  The 
structure  of  the  strands  in  the  cortex,  and  even  in  the  base  of 
the  petiole,  is  often  concentric. 

Fig.  Ill,  T,  is  from  a  photograph  of  a  cortical  bundle  of 
Cycas  revoluta.  The  center  of  the  bundle  is  composed  almost 
entirely  of  the  large  tracheids  of  the  primary  wood,  which  is 
surrounded  by  the  radially  arranged  secondary  woqd  and 
phloem.  Higher  up,  in  the  lower  part  of  the  petiole,  the  bun- 
dles lose  most  of  their  secondary  wood  and  assume  mesarch 
structure.  This  is  well  seen  in  Fig.  Ill,  U,  which  may  be 
compared  with  Figs.  109,  K,  and  110,  P.  A  striking  feature 
of  the  bundle  at  this  stage  is  that  the  primary  wood  is  mostly 
centripetal,  and  has  consequently  a  markedly  cryptogamic  ap- 
pearance. 

Before  discussing  further  the  significance  of  the  peculiar 
structure  of  the  foliar  traces  of  the  Cycads,  it  will  be  con- 
venient to  refer  to  an  interesting  discovery  made  by  Scott.7 
Mesarch  bundles  have  been  found 'by  him  in  the  central  cylinder 
of  the  peduncle  of  the  cone  of  Stangeria  paradoxa  and  certain 
other  Cycads.  The  conservatism  of  reproductive  organs  is  rec- 
ognized by  the  universal  use  made  of  them  in  botanical  classi- 
fication. It  is  Scott's  opinion  that  in  the  conservative  repro- 
ductive branches  (i.  e.,  cones)  of  certain  living  Cycads  the  an- 
cestral type  of  bundle  is  retained.  Hence  he  believes  that  the 
caul  in  e  central  cylinder  of  the  more  or  less  remote  ancestors 
of  the  living  Cycads  must  have  had  a  Structure  similar  to  that 
of  the  stem  of  Lyginodendron.  This  hypothesis  is  borne  out 
by  the  fact  that  the  course  of  the  leaf -traces  in  the  cones  of 
Cycads  is  the  same  as  in  the  seedling  of  the  genus  Cycas,  and 
in  the  vegetative  stems  of  the  extinct  group  of  Cycad-like  Ben- 
netti tales ;  for  they  pass  directly  into  the  leaves  (sporophylls) 
and  do  not  form  girdles.  Jeffrey  10  has  pointed  out  a  similar 


306  MORPHOLOGY  OF  ANGIOSPERMS 

conservatism  in  the  structure  and  course  of  the  bundles  in  the 
cones  of  Equisetum. 

Leaf -traces  are  likewise  extremely  conservative  in  structure, 
for  where  cenogenetic  modifications  are  present  in  the  ordinary 
cauline  strands,  the  primitive  type  of  fibrovascular  bundle  is 
often  retained  in  the  leaf-traces,  as  well  as  in  the  reproductive 
axis  and  in  the  seedling.  Ancestral  features  are  retained  more- 
over in  the  leaf-traces,  especially  those  of  the  cotyledons,  long 
after  they  have  disappeared  elsewhere.  Hence  it  is  assumed 
that  the  mesarch  structure  of  the  foliar  bundles  of  the  Cycads 
supplies  a  further  argument  for  their  derivation  from  ances- 
tors like  Lyginodendron. 

The  fact  that  cycadean  leaf-traces  are  often  concentric  in 
the  lower  part  of  their  course  has  been  used  as  an  argument 
by  Worsdell16  in  favor  of  the  hypothesis  that  the  cauline  bun- 
dles of  the  ancestors  of  the  Cycads  were  originally  concentric. 
This  argument  seems  to  have  the  same  force  as  the  similar  argu- 
ment in  the  case  of  the  mesarch  collateral  bundles ;  and  the  fact 
that  concentric  strands  are  comparatively  rarely  present  in  the 
living  Cycads  is  probably  due  to  the  concentric  condition  being 
further  in  the  phylogenetic  background.  The  structure  of  the 
conservative  trachea ry  strands  of  the  leaves  and  peduncles  of 
the  Cycads  would  seem  to  point  to  a  more  immediate  ancestry 
with  the  general  organization  of  Lyginodendron,  derived  in 
the  remoter  past  from  forms  like  Medullosa. 

BENNETTITALES 

The  external  vegetative  features  and  the  reproductive  organs 
of  this  interesting  group  have  already  been  dealt  with  in  the 
companion  volume  treating  of  Gymnosperms  (p.  142).  Al- 
though their  reproductive  organs  differ  very  strikingly  from 
those  of  any  living  Cycads,  the  fibrovascular  anatomy  of  the 
Bennettitales  is  strikingly  cycadean  (Scott15).  They  possessed 
a  large  cycadean  pith  penetrated  by  mucilage  canals  and  bound- 
ed by  a  thin  fibrovascular  ring.  The  continuity  of  the  fibro- 
vascular zone  was  broken  at  intervals  opposite  the  large  leaf- 
traces,  which  separated  in  the  cortex  into  arcs  of  bundles  pass- 
ing directly  into  the  leaves.  The  direct  course  of  the  foliar 
bundles  is  to  be  compared  with  that  present  in  the  cones  only 
of  living  Cycads.  This  condition  is  probably  to  be  regarded 


COMPARATIVE  ANATOMY  OF  GYMXOSPERMS  307 

as  ancestral,  because  it  occurs  also  in  cycadean.  seedlings.  The 
foliar  bundles  of  the  Bennettitales  were  characterized  by  the 
same  peculiarities  as  those  of  the  more  modern  Cycads. 

COKDAITALES 

On  page  135  of  the  companion  volume  treating  of  Gymno- 
sperms,  the  reproductive  features  and  general  morphology  of 
tliis  interesting  alliance  are  sufficiently  described.  The  central 
cylinder  of  the  Cordaites  enclosed  a  large  pith,  and  was  charac- 
terized by  considerable  secondary  growth.  Like  the  Cycads  and 
unlike  the  Conifers  of  the  present  day,  the  secondary  wood  gen- 
erally showed  no  annual  rings.  The  wood  of  Cordaites,  in  some 
cases  at  least,  is  to  be  identified  with  Araucarioxylon  and  Da- 
doxylon,  fossil  woods  which  occur  as  far  down  in  the  strata  as 
the  Devonian.  Scott 14  has  shown  that  in  some  species  of 
Araucarioxylon  the  primary  wood  of  the  stem  was  mesarch. 
In  a  good  many  cases,  however,  the  primary  cauline  bundles 
of  Cordaites  are  only  distinguished  by  exceptionally  large  de- 
velopment as  compared  with  those  of  the  higher  living  Gymno- 
sperms.  The  leaf-traces  were  mesarch  like  those  of  the  Cycads, 
and  Scott 15  compares  the  structure  of  a  cordaitean  leaf  to  that 
of  a  pinna  of  Zamia.  Fig.  Ill,  V,  shows  the  structure  of  a 
transverse  section  of  part  of  a  leaf  of  a  species  of  Cordaites. 

The  organization  of  the  cauline  and  foliar  bundles  of  the 
Cordaites  favors  the  view  of  their  derivation  from  a  pterido- 
phytic  ancestry  quite  as  much  as  that  of  their  reproductive 
organs.  Their  well-marked  foliar  gaps  and  their  large  leaves 
clearly  indicate  their  filicinean  affinities.  The  thickness  of  the 
woody  cylinder  and  the  freely  branching  habit  of  the  Cordaites 
indicates  a  greater  proximity  to  the  Coniferales  than  to  the 
Cycadales. 

GIXKGOALES 

The  discovery  of  multiciliate  sperms  in  Ginkgo  is  good  evi- 
dence for  the  antiquity  and  the  affinities  of  the  group.  Still, 
its  pteridophytic  features  have  suffered  very  considerable  re- 
duction as  compared  with  the  Cycadales.  Evidences  of  mesarch 
structure  are  accordingly  comparatively  scanty.  The  bundles 
of  the  stem  are  throughout  endarch,  and  even  the  leaf-traces 
show  slight  traces  of  the  presence  of  centripetal  wood.  Wors- 


308  MORPHOLOGY  OF  ANGIOSPERMS 

dell,8  however,  has  found  that  the  bundles  of  the  cotyledons 
show  fairly  well-developed  cryptogamic  wood.  Fig.  Ill,  Wf 
taken  from  Worsdell,  makes  the  truth  of  this  statement  appar- 
ent. The  anatomical  evidence  leads  to  the  conclusion  that  we 
have  in  Ginkgo  a  comparatively  modern  genus  as  compared  with 
the  living  representatives  of  the  cycadean  stock.  Distinct  foliar 
gaps  are  present,  which,  taken  together  with  the  large  leaves 
and  the  multiciliate  sperms,  point  strongly  to  a  filicinean  an- 
cestry. 

CONIFERALES 

The  Coniferales  are  the  prevailing  Gymnosperms  of  the 
present  day,  and  it  is  not  surprising  that  they  should  present 
few  anatomical  features  which  can  be  considered  ancestral. 
Their  usually  small  acicular  leaves  offer  a  striking  contrast 
to  the  large  fern-like  foliar  organs  of  the  older  gymnospermous 
groups.  On  account  of  the  peculiar  appearance  of  their  foliage 
it  is  not  to  be  wondered  at  that  they  should  have  been  associated 
by  Eenault,2  Campbell,5  and  Potonie  11  with  lycopodineous  an- 
cestors. Recent  work  on  the  anatomy  (Jeffrey19)  of  vascular 
plants  in  general  appears  to  show  that  in  the  case  of  the  Conife- 
rales the  microphyllous  habit  has  merely  an  ecological  interest ; 
for,  unlike  all  the  Lycopodiales,  they  have  well-marked  foliar 
gaps  in  their  cauline  woody  cylinder. 

The  researches  of  Worsdell  8  on  the  foliar  bundles  of  the 
Conifers  have  resulted  in  a  clear  demonstration  of  striking 
pteridophytic  features.  Fig.  112,  X,  represents  a  cross-section 
of  the  cotyledonary  bundle  of  C ephalotaxus  drupacea.  On  the 
lower  side  of  the  fibrovascular  strand  centrifugal  wood,  such 
as  is  ordinarily  present  in  the  bundles  of  the  Conifers,  can  be 
made  out.  On  the  upper  side  of  the  bundle  are  large,  thick- 
walled  elements,  which  are  to  be  compared  with  the  centripetal 
tracheids  of  the  cycadean  bundle  in  Fig.  Ill,  U.  Fig.  112,  Y, 
shows  a  longitudinal  section  of  a  cotyledonary  bundle  of  C. 
Fortunei.  On  the  left  are  some  pitted  tracheids  of  the  second- 
ary wood.  In  the  center  of  the  bundle  is  the  disorganized  pro- 
toxylem,  while  on  the  right  is  a  single  reticulated  tracheid  of 
the  ancestral  centripetal  wood.  The  cotyledonary  bundles  of 
Cephalotaxus  are  consequently  mesarch  like  those  of  the  ordi- 
nary leaves  in  Cycads,  but  show  striking  signs  of  degeneracy 


COMPARATIVE  ANATOMY  OF  GYMXOSPERMS  309 

in  the  centripetal  cryptogamic  wood.  On  the  flanks  of  the 
bundle  the  centripetal  wood  is  continuous  with  the  short-pitted 
cells  of  the  "  transfusion  tissue  "  discovered  by  Frank  in  1864. 
In  the  bundles  of  the  adult  leaves  of  most  of  the  living  Con- 
ifer ales  there  are  only  the  very  slightest  traces  of  centripetal 
wood.  Worsdell  has  reached  the  interesting  general  conclusion 
that  the  "  transfusion  tissue  which  occurs  almost  universally 
in  the  leaves  of  gymnospermous  plants  as  an  auxiliary  con- 
ducting system  has  been  phylogenetically  derived  from  the 
centripetally  formed  xylem  of  the  vascular  bundle." 

Fig.  112,  Z,  shows  the  topography  of  a  cross-section  of  a 
branch  of  Thuja  occidentalis.  The  leaves  in  this  species  are 
extremely  reduced,  especially  those  occurring  on  the  upper  and 
lower  sides  of  the  flattened  branches.  It  might  naturally  be 
expected  that  under  these  circumstances  the  foliar  gaps  would 
be  obscure  or  absent,  but  such  is  not  the  case,  for  subtending 
the  traces,  which  pass  to  the  specially  small  leaves  on  the  upper 
and  lower  sides  of  the  flattened  branch,  are  two  distinct  foliar 
lacunae.  An  examination  of  a  large  number  of  Conifers,  some 
with  a  very  considerable  xerophytic  reduction  in  the  size  of 
their  leaves,  has  shown  that  the  presence  of  foliar  gaps  is  quite 
constant  in  the  group  (Jeffrey  19).  It  is  now  known  that  foliar 
gaps  are  unfailingly  absent  in  the  tubular  central  cylinder  of 
living  and  fossil  Lycopodiales  and  Equisetales,  while  on  the 
other  hand  they  are  invariably  present  in  the  Filicales.  Hence 
it  may  be  assumed  that  the  Coniferales,  much  as  they  resemble 
the  Lycopods  in  external  appearance,  are  really  derived  from 
filiciriean  ancestors  by  adaptation  to  a  xerophytic  mode  of  life. 
The  microphyllous  habit  is  obviously  a  cenogenetic  adaptation, 
for  the  structure  of  the  fibrovascular  skeleton  plainly  indicates 
that  the  coniferous  stock  is  palingenetically  megaphyllous,  and 
thus  allied  to  the  Ferns. 

Fig.  112,  A  A,  shows  the  structure  of  the  root  of  Pinus 
Strobus.  The  cortex  and  phloem  surround  a  considerable  mass 
of  secondary  wood,  in  the  center  of  which  may  be  distinguished 
the  exarch  primary  wood.  This  feature  is  more  clearly  seen 
in  Fig.  112,  BB,  which  represents  the  center  of  the  section 
shown  in  Fig.  112,  A  A,  more  highly  magnified.  It  is  an  in- 
teresting fact,  to  which  Van  Tieghem  4  has  drawn  attention, 
that  the  mode  of  growth  of  the  primary  wood  is  the  same  in  all 


310  MORPHOLOGY  OF  ANGIOSPERMS 

the  vascular  plants,  viz.,  exarch  and  centripetal.  The  root  of 
the  Spermatophytes  is  consequently  conservative,  and  retains 
intact  ancestral  pteridophytic  features.  It  seems  phylogenet- 
ically  significant  that  the  exarch  type  of  wood,  so  typical  of 
the  Lycopods  and  their  allies,  is  always  present  in  roots,  and 
never  the  mesarch  type  so  characteristic  of  the  Fern-alliance. 
This  feature  probably  indicates  that  the  Lycopod  stock  is  an 
extremely  old  one,  a  conclusion  borne  out  by  the  fact  that  the 
Lycopsid  series  had  already  culminated  in  the  Carboniferous 
age.  It  appears  also  not  improbable  that  the  Pteropsida,  large- 
leaved  fern-like  plants,  took  their  origin  from  the  microphyl- 
lous  Jycopodinean  stock  in  remote  antiquity,  and  still  exhibit 
a  trace  of  their  origin  in  the  primary  structure  of  their  roots. 

GNETALES 

This  group  is  generally  regarded  as  the  highest  of  the  Gym- 
nosperms,  a  view  which  is  borne  out  both  by  a  consideration 
of  its  anatomy  and  its  reproductive  organs.  The  latter  show 
in  the  case  of  Tumboa  and  Gnetum  a  considerable  advance 
toward  the  condition  of  true  flowers,  and  this  advance  is  paral- 
leled by  a  reduction  in  the  amount  of  female  prothallial  tissue 
antecedent  to  fertilization.  The  Gnetales  on  the  anatomical 
side  show  indubitable  evidence  of  gymnospermous  relationship, 
in  the  presence  of  quite  typical  foliar  transfusion  tissue.  They 
are  distinguished  anatomically  from  all  other  Gymnosperms, 
however,  living  or  fossil,  by  the  presence  of  rudimentary  vessels. 

Fig.  113,  CC,  shows  the  structure  of  the  wood  in  Gnetum 
Gnemon.  The  secondary  wood  in  this  species  consists  of  tra- 
cheids  and  vessels,  the  latter  being  easily  distinguished  by  their 
larger  size.  In  some  cases  the  fact  that  direct  communication 
between  two  contiguous  vessels  is  merely  the  result  of  the  dis- 
appearance of  the  membrane  of  a  bordered  pit  can  be  made 
out.* 

*  For  list  of  literature  cited  see  end  of  Chapter  XVII. 


CHAPTER    XVII 

COMPARATIVE    ANATOMY    OF    ANGIOSPERMS* 

THE  question  of  the  relationship  of  the  two  great  divisions 
of  the  Angiosperms  has  for  many  years  been  a  matter  of  dis- 
pute. Anatomically  the  differences  between  the  Dicotyledons 
and  Monocotyledons  are  sufficiently  well  marked,  but  it  has 
not  been  easy  to  decide  from  ordinary  anatomical  data  which 
should  be  regarded  as  having  the  more  primitive  and  antece- 
dent organization.  There  can  be  little  doubt  that  the  two  groups 
are  closely  related,  for  in  addition  to  the  striking  general  re- 
semblance of  their  sporophytic  tissues  there  is  almost  an  identi- 
cal organization  of  the  male  and  female  gametophytes.  The 
Monocotyledons  have  by  some  been  regarded  as  primitive  on 
account  of  the  absence  of  a  cambium  in  their  ordinarily  closed 
bundles.  This  view  has  been  strengthened  by  statements  as  to 
their  appearing  earlier  in  the  geological  strata  than  the  Dicot- 
yledons. It  is  now  known  beyond  doubt,  however,  that  many 
of  the  earlier  cryptogamous  groups  had  well-marked  secondary 
growth,  so  that  the  absence  of  cambial  activity  is  by  no  means 
necessarily  a  primitive  feature.  Further,  a  more  careful  study 
of  plant  fossils  has  made  it  clear  that  many  of  the  remains  for- 
merly considered  to  be  Monocotyledons  are  in  reality  Pterido- 
phytes  or  Gymnosperms.  Discussion  of  these  interesting  prob- 
lems will  be  more  profitable  after  the  salient  features  of  the 
anatomy  and  development  of  the  Angiosperms  have  been  de- 
scribed. 

DICOTYLEDONS 

It  has  been  shown  by  Jeffrey  13  that  the  primitive  condition 
of  the  central  cylinder  in  the  Angiosperms  is  siphonostelic. 
The  tubular  central  cylinder  of  the  seedling  of  Ranunculus, 

*  Contributed  by  Professor  Edward  C.  Jeffrey,  of  Harvard  University. 
21  311 


312  MORPHOLOGY  OF  ANGIOSPERMS 

for  example,  is  characterized  by  foliar  gaps  such  as  are  found 
in  the  Filicales  and  Gymnosperms.  Often  in  the  seedling  of 
this  genus  there  is  present  an  internal  limiting  layer  of  the 
stelar  tissue  which  degenerates  in  the  adult.  Hence  it  may  be 
assumed,  in  the  absence  of  negative  evidence,  that  the  pith  of 
Ranunculus  belongs  to  the  same  morphological  category  as  the 
cortex.  Marie,  from  a  comparative  study  of  the  anatomy  of 
all  the  Ranunculaceae,  has  reached  the  conclusion  that  the  genus. 
Ranunculus  is  the  starting-point  from  which  all  the  other  gen- 
era of  the  order  have  been  derived.  It  follows  apparently  that 
the  central  cylinder  of  the  Ranunculaceae  in  general  is  suscep- 
tible of  the  same  interpretation  as  that  of  Ranunculus.  If  the 
central  cylinder  of  the  Ranunculaceae  be  siphonostelic  with 
foliar  gaps,  i.  e.,  phyllosiphonic,  it  may  fairly  be  assumed 
that  the  central  cylinder  of  Dicotyledons  in  general  is  to  be 
similarly  interpreted,  especially  as  foliar  gaps  are  universally 
present,  even  in  such  extreme  cases  of  xerophytic  reduction  as 
Casuarina  and  the  Cactaceae. 

There  are  some  instances  of  the  occurrence  of  concentric 
bundles  in  the  Dicotyledons,  but  they  appear  to  be  of  ceno- 
genetic  origin,  and  consequently  of  no  phylogenetic  importance ; 
for  in  the  cases  which  have  been  investigated,  the  concentric 
condition  is  ordinarily  absent  in  the  seedling,  the  leaf-traces, 
and  the  reproductive  axes.  This  feature  is  illustrated  by  Pri- 
mula farinosa,  in  which  the  bundles  of  the  seedling,  the  repro- 
ductive axis,  and  the  leaves  are  always  collateral ;  whereas  those 
of  the  older  vegetative  stem  are  usually  concentric.  Similar 
phenomena  have  been  observed  in  the  Xymphaeaceae,  Halo- 
raghidaceae,  etc. 

In  the  older  subterranean  stem  of  Ranunculus  acris  the 
fibrovascular  tube  becomes  broken  up  into  a  series  of  segments 
or  bundles  by  the  overlapping  of  the  foliar  gaps;  quite  often 
in  the  stouter  subterranean  axis  of  Ranunculus  acris  (Jef- 
frey 13)  the  foliar  bundles  tend  to  run  in  the  pith  before  passing 
out  to  the  leaves,  thus  offering  a  striking  feature  of  resemblance 
to  the  normal  course  of  the  leaf-traces  in  the  Monocotyledons. 
In  the  aerial  stem,  however,  this  feature  is  not  present,  as  may 
be  seen  in  Fig.  113,  DD,  in  which  the  arrangement  of  the 
bundles  shown  is  the  typical  one  for  the  Dicotyledons.  There 
*are  a  good  many  exceptions  to  the  rule,  however,  e.  g.,  Podo- 


COMPARATIVE  ANATOMY  OF  AXGIOSPERMS  313 

phyUum,  Gunnera,  the  Xymphaeaceae,  etc.  In  the  last-men- 
tioned cases,  the  study  of  seedlings  shows  that  the  circular  dis- 
position of  the  fibrovascular  strands  is  primitive.  In  Podo- 
phyllum  the  scattering  arrangement  of  the  bundles  is  present 
only  in  the  aerial  stem,  and  is  absent  in  the  rhizome,  as  well 
as  in  the  seedling. 

Fig.  113,  EEj  is  from  a  photograph  of  one  of  the  bundles 
of  Ranunculus  acris.  The  bundle  is  surrounded  by  a  scleren- 
chymatous  sheath,  which  is  thickest  externally.  The  xylem 
and  phloem  are  separated  from  one  another  by  a  narrow  zone 
of  cells  arranged  in  radial  rows,  indicating  that  a  slight  but 
unmistakable  cambial  activity  is  present.  The  bundle  is  con- 
sequently an  open  one.  The  protoxylem  is  obviously  the  inner- 
most part  of  the  primary  xylem,  so  the  bundle  is  endarch.  En- 
darch  nbrovascular  strands  with  secondary  growth  by  means  of 
a  cambium  are  characteristic  of  the  Dicotyledons.  In  aquatic 
Dicotyledons  (e.  g.,  the  Xymphaeaceae),  however,  secondary 
growth  is  frequently  absent. 

The  tracheary  tissue  of  Dicotyledons  with  considerable  sec- 
ondary growth  shows  a  further  division  of  labor  over  the  highest 
Gymnosperms.  In  the  oak,  for  example,  there  are  thinner  and 
thicker-walled  tracheids  as  well  as  vessels.  The  latter  have 
practically  lost  their  water-conducting  function  and  have  very 
few  extremely  small  pits  in  their  walls.  They  have  thus  been 
differentiated  for  the  purpose  of  support.  In  the  beech  this 
division  of  labor  among  the  tracheids  does  not  take  place,  for 
all  the  tracheids  are  of  the  same  type  and  have  well-developed 
bordered  pits  in  their  walls.  Strasburger  3  is  of  the  opinion 
that  the  wood-fibers  of  the  Cupuliferae  throughout  are  modified 
tracheids,  and  hence  merit  the  name  of  fiber-tracheids.  Such 
fibers  are  present  in  a  number  of  the  dicotyledonous  orders. 
In  other  cases,  according  to  Strasburger,  the  wood-fibers  are  to 
be  regarded  as  derived  from  wood-parenchyma  and  not  from 
tracheids.  In  these  instances  they  may  properly  be  called  libri- 
form  fibers.  It  is  not  clear,  however,  that  a  sharp  distinction 
can  always  be  drawn  between  the  two  sorts  of  wood-fibers. 

The  sieve-tissue  of  the  Dicotyledons  is  also  more  highly 
specialized  than  that  of  the  Gymnosperms,  for  the  sieve-tubes 
have  special  accessory  cells.  These  accessory  cells  are  derived 
from  the  same  mother-cells  as  the  sieve-tubes,  and  are  known 


314  MORPHOLOGY  OF  ANGIOSPERMS 

as  companion  cells.  Companion  cells  are  quite  absent  in  the 
Gymnosperms,  but  Strasburger  has  pointed  out  that  here  the 
marginal  cells  of  the  medullary  rays  perform  the  physiological 
function  of  companion  cells. 

The  Dicotyledons  as  a  group  are  distinguished  anatomically 
from  the  Gymnosperms  by  the  entire  absence  of  palingenetic 
pteridophytic  features  of  any  sort  in  the  fibrovascular  tissues 
of  their  stems  and  leaves.  The  bundles  are  throughout  endarch 
collateral,  except  in  the  root,  where  they  are  exarch,  as  in  all 
other  vascular  plants.  The  concentric  bundles  which  occasion- 
ally occur  in  the  Dicotyledons  are  obviously  cenogenetic,  and 
have  no  phylogenetic  significance.  Both  the  xylem  and  phloem 
of  the  Dicotyledons  show  a  marked  advance  in  differentiation 
over  all  the  Gymnosperms.  The  central  cylinder  of  the  stem 
in  the  Dicotyledons  is  characterized  by  the  presence  of  foliar 
gaps,  and  accordingly,  if  the  Dicotyledons  are  to  be  regarded 
as  derived  ultimately  from  pteridophytic  ancestors,  as  appears 
to  be  the  case,  their  descent  is  apparently  from  the  Filicales, 
either  directly  or  through  some  living  or  extinct  phylum  of  the 
Gymnosperms.  The  argument  for  descent  from  a  gymnosper- 
mous  ancestry  seems  to  gain  great  force  from  the  entire  absence 
of  pteridophytic  features  in  the  shoot  or  leaves  of  the  dico- 
tyledonous Angiosperms. 

MONOCOTYLEDONS 

The  arrangement  of  the  bundles  in  the  adult  stem  of  the 
Monocotyledons  is  very  characteristic.  Instead  of  being  dis- 
posed in  a  circle,  as  in  the  Dicotyledons,  they  are  scattered 
throughout  the  central  cylinder.  Fig.  113,  FF,  illustrates  this 
peculiarity.  Not  infrequently,  however,  e.  g.,  in  the  Lilia- 
ceae,  the  bundles  are  obviously  segments  of  a  fibrovascular  tube, 
just  as  is  typically  the  case  in  the  Dicotyledons.  Fig.  113,  GG^ 
shows  this  feature  in  the  rhizome  of  Clintonia  borealis.  Sub- 
tending gaps  between  the  bundles  are  to  be  seen  smaller  fibro- 
vascular strands,  which  are  leaf-traces.  In  this  example  we 
have  obviously  to  do  with  a  fibrovascular  tube  with  foliar  gaps. 
Interestingly  enough,  the  tubular  arrangement  of  the  fibrovas- 
cular elements  is  frequently  present  in  monocotyledonous  seed- 
lings, although  characteristically  absent  in  the  adult.  Hence 
it  may  be  inferred  that  the  tubular  central  cylinder  with  foliar 


COMPARATIVE  ANATOMY  OF  AXGIOSPERMS  315 

gaps  is  the  ancestral  condition  in  the  Monocotyledons.  In  some 
.  e.  g.,  Symplocarpus  foetidus,  the  pith  and  cortex  are 
continuous  in  the  seedling  through  the  foliar  gaps,  although 
they  no  longer  appear  to  be  so  in  the  adult.  An  internal  endo- 
dermis  or  stelar  boundary  is  also  sometimes  present  in  the  young 
plant,  but  has  usually  quite  disappeared  in  the  adult. 

The  typical  bundle  of  the  Monocotyledons  is  amphivasal 
concentric.  Such  a  bundle  is  shown  in  Fig.  113,  HH.  In  this 
type  of  bundle  the  tracheary  tissue  surrounds  the  phloem,  and 
not  the  phloem  the  tracheary  tissue,  as  is  generally  the  case  in 
the  Pteridophyta.  The  amphivasal  concentric  bundle  is  char- 
acteristic of  the  Monocotyledons  from  the  grasses  (Zizania, 
etc.)  to  the  orchids  (Habenaria,  Cypripedium,  etc.),  and  is 
quite  as  constant  a  feature  as  the  scattering  disposition  of  the 
fibrovascular  strands.  This  type  of  bundle  resembles  the  am- 
phicribral  concentric  bundles  of  the  Pteridophytes  in  showing 
no  evidence  of  secondary  growth.  Amphivasal  strands  are  ab- 
sent in  the  leaves  and  reproductive  axes  of  the  Monocotyledons, 
and  generally  in  the  seedlings  as  well.  Unlike  the  concentric 
strands  of  the  Gymnosperms,  they  are  accordingly  a  cenogenetic 
and  not  an  ancestral  feature,  but  on  account  of  their  widespread 
occurrence  in  the  group  have  an  important  phylogenetic  signifi- 
cance. 

Secondary  growth  has  been  supposed  to  be  entirely  lacking 
in  the  collateral  strands  of  the  Monocotyledons,  but  Queva  12 
lia-  recently  shown  that  characteristic  secondary  growth  is 
present  in  the  bundles  of  the  tuberous  base  of  the  stem  of 
the  liliaceous  genus  Gloriosa.  The  activity  of  the  cambium 
becomes  apparent  during  the  season  after  the  formation  of  the 
tuber,  when  it  is  passing  its  reserve  products  into  the  aerial 
stem.  From  the  occurrence  of  a  cambium  in  Gloriosa,  etc., 
Queva  has  drawn  the  conclusion  that  the  Monocotyledons  are 
derived  from  the  lower  Dicotyledons. 

The  most  salient  anatomical  features  of  the  Monocotyledons 
are  the  scattering  disposition  of  their  closed  fibrovascular 
strands,  and  the  presence  of  amphivasal  concentric  bundles. 
These  features,  although  practically  universal,  are  not  primi- 
tive ;  for  a  study  of  the  leaves,  reproductive  axes,  and  seedlings 
shows  often  a  dicotyledonous  disposition  of  the  generally  col- 
lateral strands.  Hence  we  may  infer  that  the  Monocotyledons 


316  MORPHOLOGY  OF  ANGIOSPERMS 

are  a  strictly  monophyletic  and  modern  group,  since  they  possess 
in  common  a  very  characteristic  mode  of  arrangement  of  bun- 
dles of  a  unique  type,  and  since  neither  the  structure  of  the 
bundles  nor  their  mode  of  disposition  is  palingenetic.  Further, 
the  evidence  of  secondary  growth  in  Gloriosa,  etc.,  would  seem 
to  indicate  that  the  Monocotyledons  have  come  off  somewhere 
from  the  Dicotyledons,  which  they  resemble  so  closely  in  their 
essential  reproductive  organs.  This  view  of  the  matter  seems 
strengthened  by  the  greater  reduction  of  the  sporogenous  tissue 
in  the  megasporangium  of  the  Monocotyledons  as  compared 
with  the  lower  Dicotyledons,  and  by  the  entire  absence  of  the 
probably  primitive  phenomenon  of  chalazogamy,  which  is  so 
characteristic  of  the  lower  Dicotyledons.  In  the  present  state 
of  our  knowledge  we  are  apparently  justified  in  considering 
the  Monocotyledons  to  be  a  modern,  strictly  monophyletic  and 
specialized  group,  derived  from  the  Dicotyledons  or  their  parent 
stock,  possibly  by  adaptation  in  the  first  instance  to  an  amphibi- 
ous mode  of  life.* 

LITEEATURE   CITED 

1.  METTENIUS,  G.  H.    Beitrage  zur  Anatomie  der  Cycadeen.  1857. 

2.  RENAULT,  B.    Cours  de  Botanique  Fossile.    Paris.  1880-1884. 

3.  STRASBURGER,  E.    Histologische  Beitrage.    III.  1891. 

4.  TIEGHEM,  P.  VAN.     Traite  de  Botanique.     Paris.  1891. 

5.  CAMPBELL,  D.  H.     Mosses  and  Ferns.    New  York.  1895. 

6.  WILLIAMSON  and  SCOTT.     Further  Observations  on  the  Organiza- 

tion of  the  Fossil  Plants  of  the  Coal-measures.  Part.  3.  Lygi- 
nodendron  and  Heterangium.  Phil.  Trans.  Roy.  Soc.  London 
B.  186:  1896. 

7.  SCOTT,  D.  H.    The  Anatomical  Characters  presented  by  the  Ped- 

uncle of  the  Cycadaceae.  Annals  of  Botany  11:  399-419.  pis. 
20-21.  1897. 

8.  WORSDELL,  W.  C.     On  Transfusion  Tissue ;  its  Origin  and  Func- 

tion in  the  Leaves  of  Gymnospermous  Plants.  Trans.  Linn. 
Soc.  London  Bot.  II.  5 :  301-319.  pis.  23-26.  1897. 

9.  POTONIE,  H.     Metamorphose  der  Pflanzen  im  Lichte  Palaeontolo- 

gischer  Thatsachen.     Berlin.  1898. 

10.  JEFFREY,  E.  C.  The  Development,  Structure,  and  Affinities  of  the 
Genus  Equisetum.  Mem.  Boston  Soc.  Nat.  Hist  5:  155-190. 
pis.  26-30.  1899. 

*  It  should  be  noted  that  the  manuscript  of  Chapters  XVI  and  XVII  was 
completed  April  1,  1902. 


B 


FIG.  10S.— A.  part  of  stem  of  Gleichenia  fiabellata;  B,  stem  of  Adiantum  pedatum  :  C, 
rhizome  ofPferi*  aquiUna  :  T>.  young  stem  of  same ;  E,  stem  of  iSelaginella  laevigata ; 
F,  central  cylinder  of  Osmunda  Claytoniana. 


FIG.  109. —  Gr,  forking  central  cylinder  of  Osmunda  cinnamomea;  H,  central  cylinder  of 
same ;  /,  same,  showing  presence  of  internal  phloem ;  J,  part  of  central  cylinder 
shown  in  7,  more  highly  magnified;  K,  mesarch  bundle  of  same;  Z,  stem  of  Hete- 
rangium  Grievii,  after  SCOTT;  x  5  :  ar,  central  mass  of  primary  wood;  ,r2,  secondary 
wood ;  ic,  inner  cortex ;  It,  leaf  trace ;  r,  adventitious  root ;  oc,  outer  cortex ;  -pet, 
petiole. 


Pte 


m      -•». 

1iiiU>"A'vV 
0 


FIG.  110. — M,  diagrammatic  transverse  section  of  stem  ofJfedulldaa  anglica,  after  SCOTT: 
acentric  strands ;  pd,  periderm ;  It,  leaf  trace  ;  X,  diagram  of  part  of  transverse 
section  of  stem  of  JftduUosa  Solmsi,  after  WEBER  and  STERZEL,  from  POTOXIE  :  pla, 
pti,  larger  concentric  strands  ;  st,  smaller  concentric  strands :  O,  transverse  section 
of  stem  of  Lyginodendron  Otiihamiitin.  after  WILLIAMSOX  and  SCOTT:  P,  part  of 
woody  zone  of  same;  ^,  same,  showing  internal  secondary  wood  and  internal 
phloem. 


m 


FIG.  111. — R,  stem  of  Zamia  fioridana ;  S,  central  cylinder  of  same;  T,  cortical  foliar 
bundle  of  Cycas  revoluta ;  l\  petiolar  bundle  of  same ;  F,  section  of  part  of  leaf  of  a 
species  of  Cordaites;  W,  cotyledonary  bundle  of  Ginkgo  biloba:  px,  protoxylem  ; 
x1,  centripetal  wood ;  a;3,  centrifugal  wood. 


BB 


FIG.  112.— X,  cotyledonary  bundle  of  Cephalotaxus  drupacea:  px,  protoxylem;  a-»,  cen- 
tripetal wood  ;  ./ 2.  centrifugal  wood ;  (/',  transfusion  tissue ;  F,  longitudinal  section 
of  cotyledonary  bundle  of  Cephalotaxus  Fortunei :  pTi,  phloem  ;  other  lettering  as  in 
-V:  Z.  small  branch  of  Thuja,  occidentalism  AA,  root  of  Pin  us  Strobus;  BB,  part  of 


HH 

FIG.  113. — CO,  wood  of  Gnetum  Gnemon;  DD,  stem  of  Ranunculus  acris\  EE,  bundle 
of  same;  FF,  aerial  stem  of  Smilax  herbacea;  GG,  part  of  subterranean  stern  of 
Clintonia  borealis;  IIH,  amphivasal  concentric  bundle  of  the  subterranean  stem  of 
timilax  herbacea. 


COMPARATIVE  ANATOMY  OF  AXGIOSPERMS  317 

11.  POTONIE,  H.     Pflaiizenpalaeontologie.     Berlin.  1899. 

12.  QUEVA,  C.     Contributions  a  Tanatomie  des  Monocotyledonees.  I. 

Les  Uvulariees  tubereuses.     Lille.  1899. 

13.  JEFFREY,  E.  C.     The  Morphology  of  the  Central  Cylinder  in  the 

Angiosperms.     Trans.  Canadian  Inst.  pp.  40.  pis.  7-11.  1900. 

14.  SCOTT,  D.  H.     Trans.  British  Assn.  Adv.  Sci.  1900. 

15.  -      — .     Studies  in  Fossil  Botany.     London.  1900. 

16.  WORSDELL,  W.  C.    The  Comparative  Anatomy  of  Certain  Species 

of  Encephalartos.    Trans.  Linn.  Soc.  London  Bot.  II.  5:  445- 
459.  pi.  4-3.  1900. 

17.  -      — .    Trans.  British  Assn.  Adv.  Sci.  1900. 

18.  FAULL,  J.  H.    The  Anatomy  of  the  Osmundaceae.     Bot.  Gazette 

32:  381-420.  pis.  14-17.  1901. 

19.  JEFFREY,  E.  C.    The  Structure  and  Development  of  the  Stem  in 

the  Pteridophyta  and  Gymnosperms.     Phil.  Trans.  Koy.  Soc. 
London  B.  195:  119-146.  pis.  6.  1902. 


'   OF  THE 

UNIVERSITY 


LITEKATUKE  CITED 

ANDREWS,  F.  M.    Development  of  the  Embryo-sac  of  Jeffersonia 

diphylla.    Bot.  Gazette  20:  423-424.  pi  28.  1895. 
ATKINSON,  G.  F.    Studies  on  Reduction  in  Plants.    Bot.  Gazette  28 : 

1-26.  pis.  1-6.  1899. 
.    On  the  Homologies  and  Probable  Origin  of  the  Embryo-sac. 

Science  13:  530-538.  1901. 
BALFOUR,  I.  B.    The  Angiosperms.    Address  to  the  Botanical  Section, 

Brit.  Assn.  Adv.  Sci.    Glasgow.  1901. 
BALICKA-IWANOWSKA,  G.  P.     Contribution  a  1'etude  du  sac  embryon- 

naire  chez  certaines  Gamopetales.     Flora   86:    47-71.  pis.  3-10. 

1899. 

BARBER,  C.  A.    On  a  Change  of  Flowers  to  Tubers  in  Nymphaea  Lo- 
tus, var  monstrosa.    Annals  of  Botany  4 :  105-106.  pi.  5.  1889. 
BARNES,  C.  R.    The  Process  of  Fertilization  in  Campanula  amer- 

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INDEX 


[The  italicized  numbers  refer  to  figures.] 


Acacia.  85,  203. 

Acanthaceae,  176,  177,  256,  269. 

Acer.  134,   136,  147:   rubrum.  52. 

Aceraceae,  20,  97.  104,  110,  248,  278. 

Aehariaceae.   249. 

Aconitum  Xapellus,  82,  99,  100,  111, 

125.  221. 
Acorns.  275. 
Acrogamy.  150. 
Actinomorphy.   15.   16. 
Adiantum    pedatum.    297,   303,    Fiy. 

108. 

Adoxa.  277. 
Adoxaceae.  259. 
Aesculus.  147. 
Agave,  25:  americana,  34. 
Aglaonema.  192. 

Agraphis.  03.  77,  84,  86;  nutans,  84. 
Agrimonia,  58. 
Aizoaceae.  244. 
Alchemilla,  87,  93,  96,  104,  151,  211, 

•21s.  2W-.   acutangula.  212:   alpes- 

tri>.  212:  alpina.  55.  .58.  59,  79,  82, 

212:  arvensis,  150,  211.  212:  "  hy- 

brida,"  212;   pastoral!*.  212.  22l  ? 

pubescens,  212;    sericata,  93.  212, 

221:   speciosa.  212. 
Alisma.   77,   136,   138,   151,   152.   195. 

196;    type  of  embryo,   188;    Plan- 

tago,  188. 
Alismaceae.    77.    97,    167.    171.    220. 

230,  2G3,  265. 
Allium,     64.     77;     canadense.     218: 

Cepa,    81:    cernuum,   218;    fistulo- 

sum,    81.   218:    odorum,    103,   217. 

818,    221:     tricoccum,    218:     ursi- 

num,  81,  218. 
Alnus.   60,   131,   132,   149,   150;    glu- 

tinosa,  30,  147. 


Aloe,  53. 

Alopecurus  pratensis,  98. 

Alsineae,  131. 

Alstroemeria,  81 ;  psittacea,  81. 

Alternation  of  generations,  288. 

Althaea,   39. 

Alyssum,  63,  65,  199. 

Amarantaceae,  46,  244. 

Amarantus  retroflexus,  21. 

Amaryllidaceae,  157,  178,  236.  238, 
264,*  266. 

Amentaceae,  241. 

Amentiferae,  60,  62,  100,  105,  112, 
113,  241. 

Amici,  143,  145. 

Amsonia,  103. 

Arnygdalus,  199,  208. 

Anacardiaceae,  248. 

Anagallis,  25;  arvensis,  46. 

Anatomy  of  Angiosperms,  311;  of 
Dicotyledons,  311;  of  Gymno- 
sperms.  296;  of  Monocotyledons, 
314. 

Ancistrocladaceae.  249. 

Andrews.  F.  M.,  64,  76,  84,  101. 

Androecium.  23. 

Anemarrhena,  209,  281. 

Anemone,  64:  nemorosa,  156.  158, 
159:  patens  Xuttalliana,  157. 

Anemonella,  100;   thalictroides,  60. 

Angiosperms.  comparative  anatomy 
of.  311:  contrasted  with  Gymno- 
sperms.  1:  embryogeny  of,  2;  fos- 
sil. 272:  gametophyte  of.  3;  geo- 
graphic distribution  of.  261 ; 
phylogenetic  relation  to  Gymno- 
sperms.  283.  to  Pteridophytes, 
284:  phylogeny  of,  280:  sporo- 
phyte  of,  2. 

333 


334 


MORPHOLOGY   OF  ANGIOSPERMS 


Anoda,  101. 

Anona,  131. 

Anonaeeae,  245. 

Antennaria,  101;   alpina,  80,  82,  92, 

95,   166,  170,  211,  212;   dioica,  80, 

82,  166,  211. 

Anther,  23;   dehiscence  of,  41. 
Anthericum,    77. 
Antherozoids,  160. 
Anthyllis  tetraphylla,  203. 
Antipodal  cells,  94,  98,  111. 
Aphyllon  uniflorum,  80,  170,  206. 
Aplectrum  hiemale,  194. 
Apocynaceae,  255,  269. 
Aponogetonaceae,  229,  263,  266. 
Aquifoliaceae,  248. 
Aquilegia,  64,  78;   canadensis,  99. 
Araceae,  10,  41,  48,  56,  77,  98,  103, 

174,  192,  233,  263,  266,  274,  275. 
Arachis  hypogaea,  203. 
Arales,  233,  263,  275,  287. 
Aralia,  277,  278;  racemosa,  74- 
Araliaceae,  65,  79,  85,  251. 
Araucarioxylon,  307. 
Archangeliea,    136. 
Archesporium    of    megasporangium, 

57;  of  microsporangium,  32. 
Archichlamydeae,    97 ;    classification 

of,    240;    geographic    distribution 

of,  266. 
Arctostaphylos,    alpina,    42;     Uva- 

ursi,  42> 
Aril,  53. 

Arisaema,  62,  77,  103. 
Aristolochia,  277. 
Aristolochiaceae,  176,  244. 
Aristolochiales,  244. 
Armeria.  103;  vulgaris,  172. 
Arum,  146,  147,  233. 
Arundina,  156. 
Arundinites,  275. 
Arundo,  275. 
Asarum,  101. 
Ascherson,  P.,  196. 
Asclepiadaceae,   30.   38,   41,   61,   132, 

157,  255,  269. 
Asclepias,  37,  55.   74,   102.   109,   122, 

124,   127,   133,   135,   146,   167,   169; 

Corimti,    82.    102,    127,    157,    159, 

167;    Syriaca,    123;    tuberosa,    82, 

85,  127* 

Asparagus  officinalis.  125. 
Asperula,  82,  202;  azurea,  202. 


Asphodelus,  53. 

Aster  novae-angliae,  100,  101. 

Astilbe,  19,  37,  39,  59,  87,  103,  108; 

japonica,  58. 
Astrapaea,  131. 
Astrocarpus,  51. 
Atkinson,  G.  F.,  75,  81. 
Arena,  80,  136;  fatua,  33,  63,  76,  98, 

192. 

Avicennia,   199;    officinalis,  80. 
Azalea  indica,  125,  129. 

Baillon,  H.  Ev  42. 

Balanophora,  50,  95,  166;  dioica,  47; 

elongata,    49,    92,    218,    210,    221; 

globosa,   48,    49,    92,   218;    indica, 

49,  92;  polyandra,  47,  49. 
Balanophoraceae,  30,  48.  55,  64,  65, 

79,  92,  170,  176,  201,  206,  243. 
Balanopsidaceae,  242. 
Balanopsidales,  242. 
Balfour,  I.  B.,  209. 
Balicka-Iwanowska,   G.  P.,  96,   102, 

103,  106,  107. 
Balsaminaceae,  248. 
Bambusa,  275. 
Barber,  C.  A.,  22. 
Barnes,  C.  R.,  24,  103,  104,  .131,  136, 

146,  14£. 

Barringtonia  Vriesei,  201. 
Bartonia,   50. 
Basellaceae.  244. 
Basigamy,   150. 
Batidaceae,  244. 
Begonia,  125,  129. 
Begoniaceae,  249. 
Belajeff,  W.,  129,   131,  138. 
Bennettitales,  anatomy  of,  306. 
Benson,   Margaret.    59*,    66,    87,    100,. 

105,  147,  148,  149,  151. 
Bentham,  G.,  227. 
Berberidaceae,  64,  245,  278,  282. 
Berberis,  41. 
Bernard.   C.   H.,   61,   79,   86,   91,   92,, 

95,  103,  154,  166,  218. 
Bessey,  C.  E.,  283. 
Betula,  60,  149,  150;   alba,  147. 
Betulaceae,  243,  278. 
Bignoniaceae.  97,  176,  177,  256. 
Billings,    F.    H.,    95,    103,    106,    107, 

111,  113,  148,  149,  200,  201. 
Bixaceae,  249. 
Blattiaceae.  250. 


INDEX 


335 


Bombacaceae.  240. 

IJorraginaceae.   131,  250,  269,  271. 

Borragmales,  258. 

Borago,  97. 

Boveri,  Th.,  182. 

Bower,  F.  0.,  288. 

Brasenia,   51. 

Braun.  A..  208.  213.  221.  227. 

Bromeliaceae,  23-5.  204.  266. 

Brongniart,  A.,  143,  227. 

Brown,  Robert,  143. 

Brunelliaceae.  246. 

Bruniaceae,  240. 

Bryophyllum,   51. 

Budding,   210. 

Burmannia   javanica,   213. 

Burmanniaeeae.  200.  238,  266. 

Burns,    G.    P.,    103,    106,    107,    113, 

170. 

Burseraceae,  247. 
Butomaceae.  229,  203.  266,  275. 
Butomus,  25.  50,  63,  75,  77,  282. 
Buxaceae.  24>. 
Byblis.  108;  gigantea,  107. 
Byxl.ee.  Edith,  129. 

Cabomba.   51. 

Cactaceae,  79,  97,  108,  147,  151,  250, 

268,  312. 

Caesalpinia.  247;   mimosoides,  203. 
Calamus.   233. 
Calandrinia   eompressa,  -J-- 
Calanthe  veratrifolia,  30,  39. 
Calceolaria,   Pavonii.    J?. 
Caldwell.  O.  W.,  30,  37,  39,  40,  63,  77, 

92.   103,  136,  167,  193. 
Calendula,  103:  lusitanica,  95,  111. 
Calla.  233:    palu-trK    /?. 
Callipeltis  cucullaria,  58,  101. 
Callitrichaceae.   247. 
Callothamnus.  23. 
Caltha.   04.   78.    137.   157;    palustris, 

60,  99,  152,  156,  173. 
Calycanthaceae.  245.  267. 
Calyceraceae.  259,  270. 
Camassia    Fraseri,    138. 
Campanales,  259.  270. 
Campanula.    25.    l.i.l.    103,    104,    131, 

130.   140:   americana,  148. 
Campanulaceae.    102,    IOC,    110,    176. 

259,  270. 
Campbell.  D.  H.,  27.  28,  48,  63,  77, 

78,  84,  89,  90,  98,  99,  133,  135,  154, 


192,   195,   196,  200,   242,  282.   285, 

287,  308. 

Candolleaceae,  259,  270. 
Canellaceae,  249. 
Canna,   110,   179;    indica,  64,   73,  81, 

105,    171,   173;    limbata.   l'f't. 
Cannabineae,  56,  148,  150. 
Cannaceae,  64,  171,  237,  204.  200. 
Cannon,  W.  A.,  33,  63,  78,  80,  98, 

136,   192. 

Capparidaceae,  57,  246. 
Caprifoliaceae,   259,   269. 
Capsella,  18,  61,  65,  94,  157,  196.  199; 

type   of   embryo,    199:    Bursa-pas- 

toris,   16,   19,  187,  197,   19S.   293; 

Heegeri,  293. 

Carboniferous  Monocotyledons.  273. 
Car  ex  acuta,  74,  124,  128. 
Caricaceae,   249. 
Carlson,  G.  W.  F.,  293. 
Carpel,  24;  morphology  of.  22. 
Carpinus,  60,  66,  87,  110,   131,   148, 

150;   Betulus,  105.   147. 
Carum  bulbocastanum,  206. 
Carya,  148;  olivaeformis,  149. 
Caryocaraeeae,  249. 
Caryophyllaceae,    57,    97,    103.    179, 

244.  207. 

Cassia  lentiva,  Jt2. 
Castanea.    60,'  102,    109,    110:     vul- 

garis,  100,  105. 
Casuarina,  28,  59,  60,  66,  79,  87,  92, 

101,   102,   105,   109,    149.   150,   157, 

167,  312;   suberosa,  I.J.9. 
Casuarinaceae,  97,  242. 
Casuarinales.  242. 
Celakovsky.  L.  F.,  8,  9,  52.  288. 
Celastraceae.  248. 
Celastrales.  248. 
Celastrus,   53. 

Centrolepidaceae.  235,  264.  276. 
Centrosomes,  153. 
Centrospermae,   244. 
Centrospennales,    244. 
Cephalotaceae,  246. 
Cephalotaxus,    drupacea,    308.    Fig. 

112:    Fortunei,  308,  Fig.  112. 
Ceratophyllaceae,  157,  170.  245.  207, 

282. 
Ceratophyllum,  177,  208:  demersum, 

157,  201:  submersum,  82.  177. 
Cercis,  203:  siliquastrum,  2<)3. 
Chalazogamy,  149. 


336 


MORPHOLOGY  OF  ANGIOSPERMS 


Chamberlain,  C.  J.,  28,  30,  31,  52,  58, 

60.  11,  79,  81,  87,  94,  95,  100,  101, 

132,   133,   134,   135,    136,   138,   151, 

199. 

Chauveaud,  G.  L.,  55,  123,  217,  221. 
Cheiranthus  Cheiri,  221. 
Chenopodiaceae,  57,  103,  179,  244. 
Chlaenaceae,  249. 
Chloranthaceae,  242. 
Chlorophytum  Sternbergianum,  81. 
Chodat,  R.,  79,  91,  92,  95,  103,  166, 

218. 
Chromatin,  behavior   during  fusion, 

153. 
Chromosomes,    128,    211;    reduction 

of,  80,  128. 
Chrysanthemum,      38 ;      Leucanthe- 

mum,  61. 

Cicer  arietinum,  204- 
Cistaceae,   56,  249. 
Citrus,    147,    214;    Aurantium,    213, 

221. 

Cladosiphonic,   298. 
Clematis,   64,   84,  99,   122,   156;    cir- 

rhosa,  60. 
Clethraceae,  253. 

Clintonia  borealis,  314,  Fig.  113. 
Clusia  alba,  221. 
Cneoraceae,  247. 
Cnicus,  157;   arvensis,  17. 
Coalescence,  12. 
Cochlospermaceae,  249. 
Coelebogyne,  214;  ilicifolia,  213,  221. 
Coffea  arabica,  221. 
Colchicum  autumnale,  147. 
Columelliaceae,  256. 
Combretaceae,  250. 
Commelina,  77,  99;   stricta,  63. 
Commelinaceae,  56,  63,  196,  235,  264, 
•    266. 
Compositae,    12,    15,   16,    18,   22,   24, 

33,  46,  58,  61,  87,  95,  97,  100,  101, 

102,   103,   111,   113,   131,   157,   174, 

259,  270,  271. 
Conard,  H.  S.,  201,  207. 
Conducting  tissue,  25. 
Coniferales,  286;  anatomy  of,  308. 
Connaraceae,  246. 
Conrad.  A.  H.,  31,  34,  58,  60,  66,  79, 

94,   147. 
Contortae,  255. 
Convallaria,    63,    64,    77,    133,    136; 

majalis,   33,   81;    multiflora,    125. 


I    Convolvulaceae,  131,  269. 
1    Conyza,  96,  101. 
Cook,   M.   T.,    176. 
Corallorhiza   multiflora,   195. 
Cordaitales,  anatomy  of,  307. 
Cordaites,  Fig.  111. 
Coriariaceae,  248. 
Corn,  xenia,  180. 
Cornaceae,  251. 
Cornucopiae,  63,  98. 
Cornus,  147;  sanguinea,  125. 
Correns,  C.,  180. 
Corry,  T.  H.,  132. 
Corydalis,  cava,  172,  173,  206;  lutea, 

206;  nobilis,  206. 
Corylus,  60,   8v,   132,   148,   149,   150; 

americana,  30,  31 ;   Avellana,  105, 

147. 

Corynocarpaceae,  248. 
Coryphanthe,  231. 
Costus,  77,  171. 

Cotyledon,   phylogeny   of,   208;    sin- 
gle in  Dicotyledons,  206;  three  in 

Dicotyledons,  208. 
Coulter,  J.  M.,  36,  37,  38,  60,  61,  65, 

81,  87,  88,  131,  135,  136,  151,  169, 

170,  193,  199,  290. 
Crassulaceae,   246. 
Crataegus,  199. 
Cretaceous   Dicotyledons,   276,   278; 

Monocotyledons,  273. 
Crinum,  53;  eapense,  178. 
Crocus,  94,  99,  104,  146,  147. 
Croomia,  266;  japonica,  266;  pauci- 

flora,  266. 

Crossosomataceae,  246. 
Crucianella,    82,    85;    macrostachya, 

86. 
Cruciferae,   18,  57,  65,  97,  157,  246, 

267. 

Cucurbita,  150,  151,  179,  205. 
Cucurbitaceae,   131,   174,  259,  270. 
Cunoniaceae,  246. 
Cuphea,  63,  96,  104. 
Cupuliferae,.  97,  131,  174,  313. 
Cuscuta,  174,  206. 
Cycadales,  286;    anatomy  of,  304. 
Cycadofilices,      109;      anatomy      of, 

Cycads,  301. 

Cycas,  305;   revoluta,  305,  Fig.  111. 
Cyclamen,  europaeum.  ^2;  persicum, 
206. 


INDEX 


337 


Cyclauthaceae,  232,  263,  266,  275. 

CyL-lanthera.   28. 

Cyclic  Aeries,  12,  228,  234. 

Cy donia,  59. 

Cymbalaria.    158. 

CynaiK-lmm.  55.  124. 

Cynocrambaceae,  244. 

Cynomoriaceae,  250. 

C'ynomorium,  76,  147,  201. 

Cyperaceae,  122,  230..  265.  275. 

C  ypripediuni,  132,  238,  239,  315;  bar- 

batum,  81;  spectabile,  133. 
Cyrillaceae.  248. 
Cyrtosperma.  263. 
Cystisus,  203;  Laburnum,  203. 
Cytinaceae.  206. 

Dadoxylon,  307. 

Damascena,   158. 

Datiscaceae,  249. 

Datura.  38.  157,  158:  laevis,  136, 
151.  105.  178. 

DeCandolle.  A.  P.,  9,  227. 

Definitive  nucleus.  See  Endosperm 
nucleus. 

De  Jussieu.  A.  L..  227. 

Delphinium,  64,  70,  78,  84,  87;  ela- 
tum.  156:  exaltatum,  100;  tri- 
corne,  60,  87,  99,  154. 

Delpino.  F..  282. 

De  Vrie>.  H..  180,  292,  293. 

Diapensiaceae,  253,  269. 

Dichapetalaceae.  247. 

Dicotyledons,  4,  11;  anatomy  of, 
311:  cyclic  number  of,  5;  embryo 
of,  4.  V,  196;  fossil,  276;  leaves 
of.  5,  6:  in  Lower  Cretaceous, 
270:  in  Tertiary.  278:  in  Upper 
Cretaceous,  278;  phylogeny  of, 
2s  1:  prophyllum  of,  7;  roots  of, 
7 :  -eed  germination,  6 ;  vascular 
bundles  of.  4. 

Dieffenbachia,  77,  84,  192. 

Digitalis,  136. 

Dilleniaceae.  249. 

Diodia.   104.   Ill;    virginiana,   102. 

Dioecism,  20,  21. 

Dioscoreaceae,  196,  236.  264,  266, 
274.  276. 

Dip-aceae.  18,  102,  269. 

Dipterocarpaceae,  249. 

Dodel.  A.,  217,^221. 

Doronicum,  101;  macrophyllum,  32. 


Double   fertilization,    155,   156,   160, 

180:  nature  of,  182. 
Draba  verna,  293. 
Dracaena,  237,  285. 
Droseraceae,  240. 
Ducauip,  L.,  65,  74,  79,  85. 
Duggar,  B.  M.,  31,  37,  136. 
Dumee  et  Malinvaud,  58,  64. 
Dunn,  Louise  B.,  100. 

Ebenaceae,  254. 

Ebenales,  254,  269. 

Egg,  93,  145;  apparatus,  93;  rest  of, 
169. 

Ehrarta  panicea,  98. 

Eichhornia,  80,  94,  95,  135,  136;  cras- 
sipes,  73,  81,  135,  170. 

Eichler,  A.  W.,  8,  15,  51,  52,  227,  241. 

Elaeagnaceae,  250. 

Elaeocarpaceae,  249. 

Elatinaceae,  249. 

Elatine  hexandra,  125. 

Elmore,  C.  J.,  218. 

Elodea,  157,  170. 

Elfving.  F.,  124,  132,  148. 

Embryo,  187;  Alisma  type,  188;  An- 
giosperms  and  Gymnosperms  con- 
trasted, 2:  Capsella  type,  199; 
degree  of  development,  205;  de- 
partures from  type,  195;  Lilium 
type,  193;  Monocotyledons  and 
Dicotyledons  contrasted,  4,  7:  of 
Dicotyledons,  196;  of  Monocoty- 
ledons, 188;  Orchid  type,  194; 
origin  of,  144;  Pistia  type,  192. 

Embryo-sac,  chambered,  175.  176; 
enlargement  of,  103,  109;  number 
of,  86:  nutritive  jacket,  103,  109; 
nutritive  mechanism,  108. 

Embryonal  vesicle.  143. 

Empetraceae.   248. 

Enantioblastae.  236. 

Endlicher,  S.  L.,  52,  227. 

Endosperm,  165;  continuation  of 
growth,  178:  displaced  by  em- 
bryo. 174:  division  of,  169:  feeble 
development  of,  171;  function  of, 
179:  morphological  character  of, 
181;  nature  of,  183;  nature  of  tis- 
sue. 178;  nuclear  fusions.  172: 
nucleus,  89,  166;  origin  by  free 
nuclear  division.  172:  origin  by 
Avail-formation,  174. 


338 


MORPHOLOGY  OF  ANGIOSPERMS 


Endothecium,  34. 
Endymion,  158;  nutans,  156. 
Engler,  A.,  8,  10,  11,  28,  30,  32,  227, 

228,  233,  234,  240,  242,  252,  274. 
Epacridaceae,  253,  269. 
Epigaea,  53. 
Epigyny,  14. 
Epilobium,  122. 
Epipactis,  194;  palustris,  193. 
Equisetum,  306;  telemateia,  154- 
Erianthis,  99,  281;  hiemalis,  206. 
Ericaceae,  41,  157,  253. 
Ericales,  253,  268,  271. 
Erigeron,   151,   156,   158,   169;   phila- 

delphicus,  169. 

Eriobotrya,  59,  85,  87,  96,  101. 
Eriocaulaceae,  56,  235,  264,  266,  276. 
Ernst,  A.,  89,  90,  159,  160,  193,  215, 

219,  222. 
Erodium,    103. 
Ervum  Ervilia,  204. 
Erythraea  Centaureum,  42. 
Erythrina  cristagalli,  204. 
Erythronium,    25,    53,    64,    77,    135, 

136,   146,   151,   193,  215;    albidum, 

215;    americanum,    81,    214,    222; 

dens-canis,  222. 
Erythroxylaceae,  247. 
Eucalyptus,   277,   278. 
Eucryphiaceae,  249. 
Euonymus,  53;  americanus,  221;  lat- 

ifolius,  213. 
Euphorbia,   94.    136,    151;    corollata, 

33,  49,  74,   126,  129;   dulcis,  217; 

Latliyrus,  125. 
Euphorbiaceae,  63,  97,  247. 
Exarch,  300. 
Exine,  131. 

Fagaceae,  243,  278. 

Fagales,  243,  268. 

Fagus,  59,  87,  110,  147,  151;  sylvat- 
ica,  105,  147. 

Familler,  I.,  8. 

Famintzin,  A.,  188,  196. 

Farinales,  235,  264,  276. 

Farinosae,  235. 

Fatsia  japonica,  ~4- 

Faull,  J.  H.,  299. 

Female  gametophyte,  71;  develop- 
ment of,  87;  tetrad,  71;  irregu- 
larities in,  91 ;  nuclei,  153. 

Ferraris,  T.,  94,  99,  104. 


Fertilization,  143;  double,  155,  156, 
160,  180,  182;  generative  and  vege- 
tative, 159. 

Ficaria  ranunculoides,  125,  12'J. 

Ficus,  131;  hirta,  212. 

Filicales,  286. 

Filiform  apparatus,  94. 

Fischer,  A.,  55,  58,  61,  64,  71,  77,  92, 
98. 

Flacourtiaceae.  249. 

Flagellariaceae,  235,  264. 

Floral  leaves,  origin  of,  9. 

Flower,  8;  bisporangiate,  21;  "co- 
alescence," 12;  definition  of,  9; 
"  dioecious,"  20;  hypogyny  to  epig- 
yny,  13;  morphology  of  members, 
22;  naked  to  differentiated  calyx 
and  corolla,  10;  organogeny,  16; 
primitive  vs.  reduced,  10;  spiral  to 
cyclic,  11;  symmetry,  15. 

Focke,  W.  O.,  179. 

Fol,  H.,  154. 

Forsythia,    103. 

Fossil  angiosperms,  272. 

Fouquieraceae,  249. 

Fourcroya,  131. 

Fovilla,  132. 

Fragaria,  199. 

Frank,  A.  B.,  309. 

Frankeniaceae,  249. 

Fritillaria,  77;  imperialis,  81;  Me- 
leagris,  81,  156;  persica,  123;  te- 
nella,  156. 

Frye,  T.  C.,  37,  39,  55,  61,  74,  82,  85, 
92,  102,  105,  122,  124,  127,  134, 
135,  157,  159,  167,  169. 

Fuchsia,  63,  125. 

Fullmer,  E.  L.,  33,  74,  126,   135. 

Fumaria,  246. 

Funkia,  64,  77,  215;  ovata,  125,  213, 
214,  221;  Sieboldiana,  81. 

Fusion,  behavior  of  chromatin  dur- 
ing, 153;  of  sexual  nuclei,  153; 
triple,  158. 

Fusion  nucleus,  166;  division  of, 
169. 

Gager,   C.   S.,   124. 
Galanthus  nivalis,  1$. 
Galega  orientalis,  204. 
Galeopsis  angustifolia,  ^2. 
Galieae,  97,  102,  104,  111,  113. 
Galium,  108. 


INDEX 


339 


Galtnnia.  77:   candicans,  81,  82. 
Gaim'tophyte,  42;   Angiosperms  and 

( iviimo-perms    contrasted,    2;    fe- 
male, 71 :  male,  121. 
Ganong,  \V.  F.,  14,.  214,  221. 
Gaivinia.  -/.?. 
Gaura.    :'.". 
Gi-i--<ilomaeeae.  250. 
Generative,    cell,    133;    fertilization, 

1*2:     nucleus,     132,     division     of, 

135. 

Gentiana.  50. 
Gentianaceae,   255,   269. 
Gentianak-.  21.1.  2G9. 
Geographic  distribution,  261. 
Geraniaceae.  20,  131,  247. 
Geraniales.  247. 
Geranium.   200. 
Gt-n.'i-a.-eae.  256,  269. 
Geum.   .18.    199. 
Giltay.  E..  179. 

Ginkiro.  307:  biloba,  F'KJ.  111. 
Ginkgoales.  anatomy  of,  307. 
Gladiolus,  <»<).  104. 
Glaueium   luteum.   221. 
Gleichenia.  302:  flabellata,  300,  Fig. 

W8. 
Globularia,  103,   176;   cordifolia,  42, 

107. 

Globulariaceae,  256,   269. 
Gloriosa.  315. 

Glumales.  230,  231,  264,  275. 
Glume.  231. 
Glumiflorae.  230. 
Gnetales.  anatomy  of,  310. 
Gnetum.    88,   90,   91,    283,   284,    285, 

310:  Gneinon,  310,  Fiff.  113. 
Goebel.  C..  8,  9,   15,  20,  21,   28,   30, 

33.   34.  43.  64,   122,   131,   133,    147. 

!!»»;.  20*;.  221. 
Goldflu*.  Mile.  M.,  111. 
Golin-ki.   St.  J.,   136,   137. 
Gomortegaceae.    24.1. 
Gomphrena.  91,  !>2. 
Gonyanthes  Candida,  170,  213. 
Gony-tylaceae,   249. 
Goodeniaceae.  259,  270. 
Goodyera.  193,  194. 
Gramineae.  57.  63.  77,  98,  104,  109, 

112.    113,    157,   174,   205,  230,   265, 

27.1. 

Gray.  A.,  8. 
Grcbel,  Dr.,  213. 


Grubbiaceae.  243. 

Guignard,  L.,  30,  33,  38,  39,  59,  60, 
61,  62,  63,  64,  65.  71,  77,  80,  81, 
82,  84,  85,  86,  87,  89,  90,  94,  9-5. 
96,  97,  98,  99,  101,  104,  105,  122, 
133,  136,  147,  151,  153.  154.  1.1.1. 
156,  157,  158,  159,  165,  169,  170, 
172,  178,  180,  202,  203,  204,  216, 
217.  221. 

Gunnera,  89,  90,  166,  313. 

Guttiferae,  249. 

(rvmnadenia.  77,  92,  94.  95:  conop- 
sea,  64,  82,  148,  194,  217,  221. 

Gymnosperms,  comparative  anato- 
my of,  296;  contrasted  with  An- 
giosperms, 1 ;  embryogeny  of,  2 : 
gametophvte  of,  3:  sporophyte 
of,  2. 

Gynoecium,  24. 

Gynostemium,  238. 

Habenaria,  315:  blephariglottis,  195; 

tridentata.  195. 

Haemodoraceae,  236,  264.  266. 
Hall.  J.  G.,  63,  77,  92,  95,  146,  167, 

171.  175,  192.  215,  216.  222. 
Hallier,  H...  282. 
Haloraghidaceae.  250.  312. 
Halsted,  B.  D.,  136. 
Hamamelidaceae,  246. 
Hamamelis,  30,  41:   virginiana,  147. 
Hanausek,  T.  F.,  221. 
Hanstein.  J,,  188,  196.  198. 
Hartig,  Theodore,  145. 
Hartog,  M.,  288. 
Haustoria,  104.   109,  202. 
Hautschicht.  95. 
Hebenstreitia.  177. 
Heckeria,  79,  90,  101.  167,  170.  178, 

179,  201. 

Hedysarum   coronarium.   203. 
Hegelmaier,   F.,    102,    178,    192,    206, 

207,  217,  218,  221. 
Heleocharis  palustris.  128. 
Helianthemum,  61,  122. 
Helianthus  annuus,  155.   156. 
Heliconia,  171. 
Helleborus,  64.  84;   cupreus,  60;  foet- 

idus,  82,  156. 
Helobiales.    171,   229.   231.   234.   263, 

275,  287. 
Helosis,  79,  95,  103,  166;  guayanen- 

sis,  91,  92,  218. 


340 


MORPHOLOGY  OF  ANGIOSPERMS 


Hemeroeallis,   64,    76,    77,    104,    135; 

fulva,  33,  74,  125,  126,  U9. 
Hepatica,  30,  38,  53,  94,  99,  100. 
Hernandiaceae,  245. 
Hesperis,  136. 
Heterangium,  300,  301,  302;  Grievii, 

300,  Fig.  109. 
Hibiscus,  156. 
Hicoria,  148. 
Hill,  T.  G.,  99,  192. 
Himantoglossum,  156;  hircinum,  82. 
Hippeastrum  aulicuin,  148. 
Hippocastanaceae,  248. 
Hippocrateaceae,  248. 
Hippuris,  55,  64. 
Hofmeister,   W.,    18,   32,   47,   48,   49, 

51,  53,  71,  94,   101,  106,   125,   132, 

143,   146,   147,   148,   176,   178,   181, 

206,  221,  222. 
Holferty,  G.  M.,  63,  76,  77,  78,  96, 

176,  192. 

Holm,  Theodore,  282. 
Homalomena,  263. 
Hooker,  J.  D.,  227. 
Houstonia,  55,  202. 
D'Hubert,  E.,  79,  108,  147,  151. 
Humiriaceae,  247. 
Humphrey,   J.   E.,   64,   77,    104,   154, 

171,  173,  192. 

Hyacinthus  orientalis,  74,  75. 
Hydnoraceae,  244. 
Hydrocaryaceae,  250. 
Hydrocharitaceae,  157,  171,  229,  230, 

263,  265,  275. 

Hydrophyllaceae,  176,  256,  269. 
Hydrostachyaceae,  246. 
Hypericum,  24;  calycinum,  18. 
Hypogyny,  13,  14. 
Hypophysis,  188,  198. 

Icacinaceae,  248. 

Ikeda,  T.,  77,  96,  99,  104,  111,  112, 

153,  157,  158,  174. 
Impatiens,  131,  205. 
Integument,  53. 
Intine,    131. 

Iridaceae,  64,  236,  264,  265,  276. 
Iris,  77,  99,  155;   sibirica,  217,  221; 

squalens,  81;  stylosa,  64. 
Irmisch,  T.,  206. 
Isobilaterality,  16. 
Isoetaceae,  285. 
Isoetes,   196,   284,   285,  287. 


Jasminum,  95. 

Jeffersonia,  64,  76,  84;  diphylla,  101. 

Jeffrey,    E.    C.,    214,    215.    222,    281, 

296,   297,  298,   300,   301,   303,   304, 

305,  308,  309,  311,  312. 
Johnson,  D.  S.,  79,  89,  90,  101,  104, 

105,    136,    137,    153,    166.    167.   168, 

170,  176,  178,  179,  200,  201,  242. 
Johnson,  T.,  47,  55. 
Jonsson,  B.,  221. 
Jordan,  K.  F.,  293. 
Juel,  H.   O.,   73,   74,  76,   80,   82,  92, 

101,   124,   126,   128,   129.    147,    166, 

170,  201,  211. 

Juglandaceae,  46,  157,  243.  278,  284. 
Juglandales,  243,  268. 
Juglans,  91,  146,  147,  148,  150,  156, 

157,    158;    cinerea,    149:    cordifor- 

mis,  60,  79,  84,  87;   nigra.  92,  96; 

regia,  90,  149. 

Juncaceae,  236,  264,  265,  276. 
Juncaginaeeae,    196,    229,    230,    263, 

265,  275. 

Juncagineae,  171. 
Juncus,  121. 

Jurassic  Monocotyledons.  273. 
Justicia,  131. 

Kamienski,  F.,  206. 

Karsten,  G.,  60,  79,  84,   87.   91,  92, 

96,  157,  158,  284. 
Kauffmann,  N.,  28. 
Kerner,  A.,  42. 
Klebs,  G.,  288,  289. 
Koch,  L.,  80,  206. 
Koeberliniaceae,  249. 
Kolliker,  A.,  292. 
Kornicke,  F.,  180. 
Koerhicke,  M.,  63,  81,  137. 
Korschinsky,  S.,  292. 

Labiatae,  16,  24,  104,  106,  176,  256, 

269,  271. 
Labiatales,  258. 
Lacistemaceae,  242. 
Lactoridaceae,  245. 
Land,   W.   J.    G.,    29,    82,    151,    155, 

156,  160,  169,  Figs.  35  and  36. 
Lang,  F.  X.,  107,  108. 
Lang,  W.  H.,  288,  289. 
Lappa,   122. 

Lardizabalaceae,  245,  267. 
Larix  europaea,  154- 


INDEX 


341 


Lathyrus.  136;  heterophyllus,  204; 
odoratus,  204. 

Lauraeeae.  24.5.  207. 

Laurus.  277. 

La\v>on.  A.  A.,  129. 

Leaves.  Monocotyledons  and  Dicot- 
yledons contrasted,  5,  6. 

Leavitt.  R.  G.,  193,  194. 

I.rrvtliidaeeae.    250. 

Leemvenhoek.  A..  213. 

Leguminosae.  15,  16,  20,  55,  65,  97, 

174.  202.   240.   207,   279;    embryos 
of.  2n2. 

Legmninosites,  277. 

Leitneriaceae.  242. 

Leitneriales,  242. 

Lenma.    10,   30,    39,    63,    77,   92,    95, 

103.136.107.193:   reduced  flowers.. 

10:  minor.  37.  40. 
Lemnaceae.  233.  234.  263,  265. 
Le  Monnier.  G..   181,   182. 
Lennoaceae.  253. 
Lentibulariaceae,  250. 
Lepidium,  157. 
Leptosiphon,   103. 
Leucojum  vernum,  81. 
Lilaea,  28,  46,  99;   subulata,  27.  47, 

196.   2vi. 
Liliaceae.    64.    70.    82.    97,    103,    109, 

1.17.    174.    193.   209,   236,  264,   265, 

274.  270. 

Liliales.  230.  204.  276. 
Liliiflorae.  236. 
Lilium.    2*.   4*.    5&    (54.    7*3.    /7.    *0. 

8/,  Si   '.'-->.   !»7.   104.   123,    134.    135. 

l.SO.    137.    140.    151.    1-37.    159.    101. 

1»J9.    193.    1U5:    type    of    embryo, 

193:     auratum.    13 'f.    138;     candi- 

dum,  61.  81.  86,  130.  131;  153.  !•!}: 

croceum.   81:    Martagon,   81.    1;?. 

130.  13',.   150.    158.   221:    philadel- . 

phicum.    29.   5't.   61.    81,   Fig*.    •',:> 

and    36,    88.    135.    157.    160,    193; 

pyrenaicum.  156;  tigrinum,  16,  81, 

13'h  135.  157. 
Limnanthaceae.  248. 
Limnocharis,  63.  77,  92,  95.  167,  171. 

175.  170.    192;    emarginata,    140. 
21.1.  210.  222. 

Linaceae.  247. 
Linum.  103. 

Liriodendron.  277.  278. 
Listera,.  194;  ovata,  82,  193,  194. 


Lloyd,  F.  E.,  55,  58,  61,  80,  82,  85, 

86,  97,  101,  102,  104,  108,  202. 
Loasaceae,  176,  249. 
Lobelia,  80,  103,  111. 
Lobeliaceae,  24,  30,  48,  58,  106,  110. 
Loganiaceae.  255.  269. 
Longo,  B.,  150. 
Lonicera,  80;  coemlea,  125. 
Loranthaceae,   55,   65,   97,    104.    110, 

176,  243. 
Loranthus,    50,    61,    85,    86,    91,    92, 

97,    177;    europaeus,   221.    pentan- 

drus,   49,  200;    sphaerocarpu-.   4^. 

50,  199,  200. 
Lotsy,  J.  P.,  28,  34.  48,  49,  50,  51r 

79,  92,  136,  166,  218. 
Luerssen,  C.,  131. 
Lupinus,  202,  204;  luteus.  205:   mu- 

tabilis,    205;    pilosus.    205:    poly- 

phyllus,    205:     subcarnosus.     205; 

truncatus,  205. 
Lychnis,  21. 
Lycium,  80. 
Lycopodiales.  286. 
Lyginodendron,    301,    302.    303.    305, 

306;    Oldhamium,    301,    302.    Fifi. 

110;  robustum,  302. 
Lygodium,  300. 
Lyon,   F.   M.,   49,   74,   94.    100.    126, 

129.  136,  151. 

Lyon,  H.  L.,  169,  201,  207.  20s.  282. 
Lysichiton,  63,  192;  kamtschatcense, 

"98,  192. 
Lythraceae,   104,   110,  250. 

Magnolia,  277. 

Magnoliaceae,    245. 

Magnus,  P.,  28. 

Mahonia  indica,  64. 

Maize,  xenia.  180. 

Male  cells,  136;  not  concerned  in 
fertilization,  161. 

Male  gametophyte.  121. 

Male  nucleus,  136,  152.  157.  166; 
change  in  size  and  form.  152; 
fusion,  153;  its  part  in  fertiliza- 
tion, 160:  movements  of.  157:  ver- 
miform, 161. 

Malesherbiaceae.  249. 

Malpighi.  M.,   143. 

Malpighiaceae.    247. 

Malva,  38. 

Malvaceae,  33,  131,  157,  249. 


342 


MORPHOLOGY  OF  AXGIOSPERMS 


Mai  vales..  249,  267. 

Mangifera  indica,  221. 

Marantaceae,  171,  237,  264,  266. 

Marattiaceae,  301. 

Marcgraviaceae,  249. 

Marie,  M.,  312. 

Martyniaceae,  256. 

Massula,  39. 

Mayacaceae,  235,  264,  266. 

Medicago,  104;   falcata,  204. 

Medinilla,  1$. 

Medullosa,  301,  302;  anglica,  301, 
Fig.  110;  Solmsi,  301,  Fig.  110; 
stellata,  301. 

Megasporangium,  46;  archesporium 
of,  57;  cauline,  46;  mother-cell, 
66:  parietal  cells,  62;  time  of  de- 
velopment, 52. 

Megaspore,  71;  germination  of,  87; 
number  of,  76;  the  functional,  84. 

Melastomataceae,  250,  268. 

Meliaceae,  247. 

Melianthaceae,  248. 

Melissa  officinalis,  4?- 

Mellink,  J.  F.  A.,  71,  84. 

Menispermaceae,  245. 

Menispermites,  277. 

Mentha,  38;  aquatica,  32,  33. 

Menyanthes,  103;  trifoliata,  32. 

Merrell,  W.  D.,  34,  35,  82,  101,  103, 
136,  137,  151,  158,  199. 

Mertensia,  136. 

Mesembrianthemum,   63. 

Metamorphosis,  8,  10,  22. 

Mettenius,  G.  H.,  304,  305. 

Microspermae,  238. 

Microsporangium,  27 ;  archespori- 
um, 32;  cauline,  28;  development 
of,  32;  mother-cells,  38;  number 
of,  29;  parietal  layers,  34;  tape- 
turn,  36;  time  of  formation,  30. 

Microspores,  121 ;  germination  of, 
132;  number  of,  125;  wall  of, 
131. 

Mimosa,  203,  247,  267,  268,  279; 
Denhartii,  216,  221. 

Mimoseae,  30,  33,  132. 

Mirbel,  C.  F.,  56. 

Mohl,  H.  von,  145. 

Monimiaceae,  245. 

Monocotyledons,  4,  11;  anatomy  of, 
314;  classification  of,  227;  cyclic 
number  of,  5;  embryo  of,  4,  7, 


188;  fossil,  272;  in  Carboniferous, 
273;  in  Cretaceous,  273;  in  Juras- 
sic, 273;  in  Tertiary,  275;  geo- 
graphic distribution  of,  262 ;  leaves 
of,  5,  6;  phylogeny  of,  281;  pro- 
phyllum  of,  7;  roots  of,  7;  seed 
germination,  6;  vascular  bundles 
of,  4. 

Monotropa,  148,  158,  206;  Hypopi- 
tys,  145,  156;  uniflora,  96*  102, 
147,  153,  157,  159,  167. 

Monotropaceae,  176. 

Moraceae,  243,  278. 

Moringaceae,  246. 

Morus  albus,  221. 

Mother-cell,  of  megasporangia,  38; 
of  microsporangia,  38. 

Mottier,  D.  M.,  52,  60,  61,  62,  76, 
77,  78,  82,  84,  87,  94,  99,  101,  103, 
124,  129,  130,  134,  136,  146,  153, 

154,  169,  199. 

Murbeck,  S.,  55,  58,  59,  79,  82,  87, 
93,  96,  104,  150,  175,  196,  211,  212, 
218,  219,  221,  285. 

Musaceae,  171,  237,  264,  266,  276. 

Muscari  neglectum,  81. 

Mutation  theory,  292. 

Myoporaceae,  256. 

Myoporum,  103,  200;  serratum,  201. 

Myosurus,  64,  99. 

Myrica,  277. 

Myricaceae,  242. 

Myricales,  242. 

Myristica,  53. 

Myristicaceae,  245. 

Myrothamnaceae,  246. 

Myrsinaceae,   254,   269. 

Myrsinophyllum,  277. 

Myrtaceae,  201,  250,  268. 

Myrtales,  250. 

Myzodendraceae,  243. 

Myzodendron,  105,  110;  punctula- 
tum,  47,  55. 

Xageli,  Cv  32. 

Xaiadaceae,   97,    157,    171,   229,   230, 

263,  265. 
Naias,  28,  41,  46, 133, 171,  192 ;  flexilis, 

27;  major,  81,  157,  165,  170,  216, 

221. 

Narcissus,  77,  99,  156. 
Xawaschin,  S.,  90,  146,  148,  149,  150, 

155,  156,  180. 


INDEX 


Xelumbo,  169,  201,  207,  208. 

Xemec,  B.,  74.  75. 

Xemophila,  130,  170. 

Xeottia,  131,  133;  nidus-avis,  82,  122; 

ovata.  33,  39. 
Xepenthaceae,  246,  268. 
Xicotiana,  80,  96,  97,  157,  158;  Taba- 

cum.  136,  147,  151,  158. 
Xigella,    99,    151,    158;    damascena, 

157.  159;   saliva,  156. 
Xolanaceae,  256,  269. 
Xothoscordon  fragrans,  213,  221. 
Xuphar,  50,  176;  lutea,  208. 
Xyetaginaceae,  96,  97,  244. 
Xyetandra,  -'/2. 
Xymphaea,    9,    22,    23,    50,    53,    176, 

201.  207:  alba,  82. 
Xymphaeaceae,    103,    110,    176,    245, 

282,  312,  313. 

Obolaria.   50. 

Ochnaceae,  249. 

Oenothera,   104;   Lamarckiana,  292; 

lata.  293. 
Olacaoeae,  243. 
Oleaceae,  97,  255. 
Oliniaceae,  250. 
Oliver,   F.   W.,   55.   80,   85,   95.    106, 

109,   111,   134,   148,   169,   177,   178, 

199. 

Onagraceae,  30,  97,   131,  250,  267. 
Onobrychis  petraea,  204. 
Ononis,    alopecuroides,    204:     fruti- 

cosa.  204. 
Opiliaceae,  243. 
Opuntia.    tortispina,    214;    vulgaris, 

214.    221. 
Opuntiales,  250. 
Orange,  213. 

Orchid,  195;  type  of  embryo.  194. 
Orchidaeeae,  15,  30,  58.  64,  97,  103, 

113,    132.    136,   147,   157,    171,    194, 

206.  234,  238,  266. 
Orehidales.  238,  264,  276. 
Orchis,    51.    77.    145.    156;    latifolia, 

l.'t-'t.    l-'to;    maculata,    33.    38,    39. 

1','f.  masctila.  82.  121.  126;  Morio, 

L't'f,  145,  221;  pallens,  64. 
Organogeny  of  flower.  16. 
Ornithogalum,    64,    97,    99:    nutans, 

91;   pyrenaicum,  61. 
Orobanchaceae,  176,  206,  256,  269. 
Orobanche,  80. 
23 


Orobus   angustifolius,   65,   204 ',    au* 

reus,  204. 
Osmunda,    302,    303;     cinnamomea, 

298,    299,   Fig.   109;    Claytoniana, 

298,  Fig.  108;   regalis,  299. 
Ostenvalder,  A.,  99,  100,  111,  221. 
Osyris,  105. 
Ovary,   24,   26. 
Overton,   E.,   71,  221. 
Overton,   J.    B.,   63,   64,   81,   82,   94, 

100,  170,  199,  212. 
Ovulary,  24. 
Ovules,     foliar,     50;     morphological 

nature  of,  51;  development  of,  53; 

forms  of,  56. 
Oxalidaceae,  247. 

Paeonia  spectabilis,  82. 

Palet,  231. 

Palmaceae,   231,   262,  266,   274,   275. 

Palmales,  231,  262,  275. 

Pandanaceae,  228,  262,  266,  273.  275. 

Pandanales,  228,  231,  262,  275. 

Papaver,  136;   orientale,  65. 

Papaveraceae,  65,  246. 

Papilio.  247,  267. 

Parietales,  249. 

Paris  quadrifolia,  159,  169. 

Parthenogenesis,  210. 

Passiflora,   131. 

Passifloraceae,  249. 

Payer,  J.  B.,  16,  20. 

Pechoutre.  F.,  59.   199. 

Pedaliaceae,   97,   106,   110,    176,   177, 

256,  269. 
Pedicularis,    106. 
Penaeaceae,  250. 
Pentaphyllaceae,  248. 
Peperoniia.  79,  88,  90,  136,  137,  153, 

178,    179.   200:    pellucida,  89,   166, 

168,  178,  200,  242.  284. 
Pepo  macrocarpus,  143. 
Perigyny,  13,  14. 
Perisperm,  103;  function  of,  179. 
Peristylis  grandis.  194. 
Personales.  15,  24,  258. 
Petasites,  101. 
Petit-Thouars.   213. 
Peucedanites,  277. 
Pfeffer,  W..   19. 
Pfitzer.  E.,.  194. 
Phajus,  156. 
Phalaenopsis  grandiflora.  194. 


344 


MORPHOLOGY  OF  ANGIOSPERMS 


Phaseolus,  179,  208;  multiflorus, 
204. 

Philydraceae,  235,  264. 

Phlox  Drummondii,  113. 

Phyllocactus,  108. 

Phragmites,   275. 

Phrymaceae,  256. 

Phylloglossum,  300. 

Phyllosiphonic,  298. 

Phylogeny  of  Angiosperms,  280. 

Phytelephas,  178,  231,  262. 

Phytolacca,  179. 

Phytolaccaceae,   103,   179,  244. 

Pinguicula  vulgaris,  42- 

firms,  160;  Strobus,  112,  309. 

Piper,  79,  90,  167,  178;  medium,  168. 

Piperaceae,  46,  56,  79,  103,  178,  179, 
201,  242. 

Piperales,  242,  287. 

Pirolaceae,  253. 

Pirotta,  R.,  150. 

Pirus  Malus,  15,  221. 

Pistia,  178,  192,  195,  201,  263,  275; 
type  of  embryo,  192. 

Pistil,  25. 

Pisum  sativum,  204. 

Pittosporaceae,  246. 

Placenta,  25. 

Plantaginaceae,  102,  106,  176,  258, 
271. 

Plantaginales,   258,   269. 

Plantago,  269;   Ifcnceolata,  107. 

Platanaceae,  246. 

Plumbaginaceae,  254. 

Poacites,  275. 

Podophyllum,  53,  282,  313;  pelta- 
turn,  31,  82,  124. 

Podostemonaceae,   246. 

Polar  nuclei,  92;   fusion  of,  95. 

Polemoniaceae,  103,  256,  269. 

Polemoniales,  258. 

Pollen  mother-cell,  division  of,   126. 

Pollen-tube,  143;  branching  of,  148; 
development  of,  146;  discharge  of, 
152;  entrance  into  sac,  151;  in 
cleistogamous  flowers,  146;  Prop- 
fen,  148;  time  between  pollination 
and  fertilization,  146. 

Pollination,  relation  to  endosperm, 
169. 

Pollinium,  132. 

Polyembryony,  213. 

Polygalaceae,  104,  110,  247. 


Polygonaceae,  46,  56,  179,  244,  267. 

Polygonales,  244. 

Polygonum,   94;    divaricatum,   94. 

Polypompholyx,  108. 

Polystelic,  297. 

Pontederia,    104,    146,    151;    cordata, 

81. 
Pontederiaceae,    34,    37,    63,    77,    78, 

97,  235,  264,  265. 
Populus,  52,  133,  277,  278;   monilif- 

era,  30,  31;  primaeva,  276;  trem- 

uloides,  60. 
Portulaca,   143. 
Portulacaceae,  244. 
Potamogeton,  63,  76,  77,  96,  97,  104, 

136,    176,    192;    natans,   78;    folio- 

sus,  33,  62,  78. 
Potamogetonaceae,     229,     230,     234, 

263,  265,  274,  275. 
Potentilla,   18. 
Pothos  longifolia,  148. 
Potonie,  H.,  300,  303,  308,  Fig.  110. 
Prantl,  K.,  8,  56. 
Primula  farinosa,  312. 
Primulaceae,  19,  103,  254,  269. 
Primulales,  254,  269. 
Principes,  231. 
Pringsheim,  N.,  288. 
Proangiosperms,  277,  281,  283,  286. 
Proembryo,  188. 
Propfen,  148. 

Prophyllum,  Monocotyledons  and  Di- 
cotyledons  contrasted,   7. 
Proteaceae,  131,  243,  268,  278. 
Proteales,  243. 
Proteophyllum,  277. 
Protocorm,  209. 
Protolemna,  275. 
Protostelic,  297. 
Prunus  Cerasus,  125. 
Pseudo-monocotyledons,  206. 
Pseudo-polyembryony,  221. 
Psilotum  triquetrum,  154. 
Pteridophytes,  anatomy  of,  296. 
Pteris   aquilina,   297,   298,   301,   303, 

Fi(j.  108. 
Punicaceae,  250. 
Purkinje,  J.  E.,  34. 
Pyrethrum,    85,    87;    balsaminatum, 

61. 
Pyrola    rotundifolia,    42,     secunda, 

206;  uniflora,  42. 
Pyrolaceae,  176. 


INDEX 


Quercus,  34,  66,  79,  94,  147,  148,  208; 

Robur,    147;    velutina,   31,   58,   60, 

147. 

Queva,  C.,  281,  315. 
Quiinaceae,  249. 

Eafflesiaceae,  244. 

Ramondia  pyrenaica,  -'t2. 

Ranales,  245..  287. 

Ranunculaceae.  21,  60,  64,  78,  84,  99, 

102.   Ill,    153,   157,   158,   169,  245, 

267,  2*2.  312. 
Ranunculus,  11,  16,  36,  37,  51,  55.  64, 

7*.  87,  100,  131,  136,  151,  158,  170, 

199,  311.  312:    flowers  of,   11,   16; 

abortivus,  60:  acris,  312,  313,  Fig. 

113:     Cymbalaria.     157;     Ficaria, 

206,  207,    282:     Flammula.     156; 
multifidus,  65,  88;  septentrionalis, 
61. 

Rapateaceae.  235,  264. 

Ray.  John.  227. 

ReiVhenbach,  H.  G.,  132. 

Renault.  B.,  308. 

Reseda,  20.  156:  odorata.  173. 

Resedaceae.  57,  157,  246. 

K«'-t  iaceae,  56. 

Restionaceae.  235.  204.  276. 

Reversion,  22. 

Rhamnaceae.  249. 

Rhamnales.  249. 

Rhinanthus,  106. 

Rhizophoraeeae,  250. 

Rhododendron,  132. 

Rhoedales.  246. 

Rhopalocnemis,  79,  92,  136;  phal- 
loides,  28,  34,  49,  51. 

Ricinus.  24.  170. 

Riddle.  Lumina  C.,  63,  65,  199. 

Robinia.    147. 

Rohrbach.  P..  28. 

Romulea,  94,  99,  104. 

Root,  Monocotyledons  and  Dicoty- 
ledons contrasted.  7. 

Rosa,  18,  84,  87,  221.  247;  livida,  58, 
221. 

i:«-ii<-eae.  59,  60,  62,  63,  87.  199,  246, 

207.  27!». 
Resales,  246. 
Rosanoff,  S.,  33.  132. 
Rose.  J.  X.,  135^  136. 
Rosenberg,  O.,  36,  37,  74.  77,  81.  122, 

124. 


Rubiaceae,    18,   58,   61,   80,   97,    102, 

111,  113,  202,  259,  269. 
Rubiales,  259,  269. 
Rubus,  18,  59. 
Rudbeckia  speciosa,  156. 
Rumex,  21;  Patientia,  125. 
Ruppia,  196,  285;  rostellata,  175. 
Ruta,  97;  graveolens.  62. 
Rutaceae,  20,  247. 

Sabiaceae,  248. 

Sachs,  J.,  15. 

Sagittaria,  96,  104,  135,  136,  137,  169, 

175.  176;  variabilis,  152,  154,  175, 

188,  ^89,  191. 
Salicaceae.  97,  242. 
Salicales,  242. 
Salix.  52,  60,  87,  94,   136,   151,  199, 

277,  278;  glaucophylla.  30,  58,  79, 

95;  petiolaris,  28,  57,  95. 
Salvadoraceae,  255,  269. 
Salvia,  95,  97 :  pratensis,  85. 
Sambucus,  136. 
Sanguisorba,  58. 

Santalaceae,  55,  105,  110,  176.  243. 
Santalales,  243. 

Santalum,  91,  94,  105;  album,  221. 
Sapindaceae,  20,  248. 
Sapindales.  248. 
Sarcodes,   25,   80,   97,   134,    169,   178, 

199;  sanguinea,  148. 
Sargant,  Ethel,  73,  81,  82,  157,  182, 

207,  209,  281,  282. 
Sarraceniaceae,  246,  268. 
Sarraceniales.  246. 
Sassafras,  41,  277. 
Saururaceae.  97,  104,  109.  176.  242. 
Saururus,    79,    104,    110,    176,    179; 

cemuus,  104,  105. 
Saxifraga  caespitosa,  125. 
Saxifragaceae,  59,  97,  246,  267. 
Scaevola,  103. 
Schacht.   H.,   55,   94,    131,    143.    144. 

145.  221. 
Schaffner.  J.  H.,  28,  38,  53,  63.  74, 

77.  81,  88,  96,   121.   126,  133,  135, 

136,    137,    138,    146.    151,    152,    153, 

154.    169,   175,   188,   189,   191,   193, 

215. 

Schleiden.  M.  J..  9.  52.  55.  144,  145. 
Schlotterbeck.  M.,  106. 
Schmid.  B..  206. 
Schnegg,  H.,  89,  90,  166. 


346 


MORPHOLOGY   OF  ANGIOSPERMS 


Schniewind-Thies,  J.,  77,  81,  84. 
Schrankia  imcinata,  221. 
Sehwere,  S.,  102,  199,  216,  221. 
Scilla,  64,  84,  156;   non-scripta,  81; 

sibirica,  81. 

Scitaminales,  237,  264,  276. 
Scitamineae,  57,  64,  77,  97,  103,  104, 

109,  171,  192,  237. 
Scrophularia  nodosa,  16,  125. 
Scrophulariaceae,    96,    97,    103,    106, 

110,  176,  256,  269,  271. 
Scleranthus  animus,  125. 

Scott,  D.  H.,  288,  300,  301,  302,  303, 
304,  305,-  306,  307,  Fig.  110. 

Scytopetalaceae,  249. 

Sedum,  51. 

Seed,  Monocotyledons  and  Dicotyle- 
dons contrasted,  6. 

Selaginaceae,  176,  177. 

Selaginella,  285,  287;  laegivata,  Fig. 
108. 

Senecio,  87,  101,  169,  199. 

Seward,  A.  C.,  273,  302;  aureus,  61. 

Sherardia  arvensis,  101. 

Shibata,  K.,  96,  102,  147,  148,  153, 
157,  159,  167. 

Shoemaker,  D.  N.,  30,  147. 

Sibbaldia  procumbens,  J^2. 

Silene,  94. 

Silphium,  34,  101,  103,  136,  137,  151, 
156,  158,  160,  199;  integrifolium, 
35,  82;  laciniatum,  82,  155. 

Simarubaceae,  247. 

Sinningia  Lindleyana,  221. 

Siphonostelic,  297. 

Slum,  65,  94,  96,  103,  199;  cicutae- 
folimn,  79. 

Sisyrinchium,  77;  fridifolium,  64. 

Smilax,  274;  herbacea,  Fig.  113. 

Smith,  Amelia  C.,  80,  170,  206. 

Smith,  Arma,  30. 

Smith,  R.  W.,  34,  37,  63,  73,  77,  78, 
80,  81,  94,  95,  135,  136,  146,  151, 
170. 

Snow,  Laetitia  Mv  160. 

Solanaceae,  136,  157,  176,  256,  269. 

Solanum,  41 ;  Lycopersicum,  42. 

Solms-Laubach,  H.,  196,  206,  293. 

Sonneratiaceae,  250. 

Sparganiaceae,  98,  228,  262,  265,  275. 

Sparganium.  112,  133,  192,  228,  229, 
233;  simplex,  47,  98,  135. 

Spartium  junceum,  203. 


Spathe,  232. 

Spathiflorae,  233. 

Spergularia  rubra,  46. 

Spermacoceae,  202. 

Spermatozoids,  136,  160. 

Sperms,  136,  160. 

Spiral  series,  11,  228. 

Spiranthes,  193. 

Sporangia,  foliar  and  cauline,  27,46; 
in  winter,  30;  periblem  origin  of, 
27,  46. 

Sporophyte,  41;  Angiosperms  and 
Gymnosperms  contrasted,  2. 

Stachyuraceae,  249. 

Stackhousiaceae,  248. 

Stamen,  23;  morphology  of,  22. 

Staminodia,  24. 

Stangeria  paradoxa,  305. 

Staphylea,  136,  I't5;  pinnata,  172. 

Staphyleaceae,  248,  278. 

Stellaria,  glauca,  125;  Holostea,  84. 

Stemona,  266. 

Stemonaceae,  236,  264,  266. 

Sterculiaceae,  249. 

Sterzel,  J.  T.,  Fig.  110. 

Stevens,  W.  C.,  124. 

Stichneuron,  266. 

Stigma,  25. 

Strasburger,  E.,  38,  43,  53,  58,  62,  63, 
64,  71,  73,  74,-  76,  77,  81,  82,  83,  87, 
92,  94,  99,  104,  121,  122,  123,  124, 
126,  128,  132,  133,  136,  138,  145, 
146,  148,  154,  157,  158.  159,  171, 
172,  173,  177,  181,  182,  183,  201, 
202,  208,  213,  214,  215,  217,  221, 
284,  294,  313. 

Strelitzia,  171. 

Strobilus,  theory  of,  288. 

Succisa  pratensis,  293. 

Suspensor,  113,  190,  192,  193,  194, 
202. 

Stylidaceae,  103,  106,  108,  110,  170. 

Stylidium  squamellosum,  107,  113. 

Styracaceae,  254. 

Sympetalae,  97;  classification  of, 
252;  geographic  distribution  of, 
268. 

Sympetaly,  13. 

Symphytum  officinale,  125. 

Symplocaceae,  254. 

Symplocarpus,  31,  37,  136;  foetidus, 
315. 

Svnanthae,  232. 


INDEX 


347 


Svnanthales.  232,  2G3,  275. 
Synapsi*.  126. 
irpy,  13. 
Synergids,  91,  94;  as  an  haustorium, 

111:  disorganization  of,  151. 
Syringa.  persica,  125;  vulgaris,  125. 

Taccaceae,  236,  264,  266. 

Tamaricaceae.  249. 

Tangl.  E..  125. 

Tapetum.  36. 

Taraxacum.   101.   102,   157,  199;   offi- 

einale.  216.  221. 

Tertiary.   Dicotyledons,  278;   Mono- 
cotyledons. 275. 
Tetrads.  71,  121,  126. 
Tetragonolobus  pur  pur  ens.  203. 
Thalia  dealbata,  171. 
Thalictrum,  63,  64..  78,  94,  199;  dio- 

icum,    100:    Fendleri,   212;    purpu- 

rascens.  100,  170,  212. 
Theaceae.  240. 
Theobroma  Cacao,  ^2. 
Thesiuni,  61,  105. 
Thomas.    Ethel    M.,    137,    152,    156, 

157.  158. 

Thuja  occidentalis,  309,  Fig.  112. 
Thunbergia.  131. 
Thymelaeaceae.  250,  268. 
Tiliaceae.  240. 
Tischler.  G.,  172. 
Todea  barbara.  209. 
Torenia,  111.  136:  asiatica,  104,  106. 
Tovariaceae,  246. 
Tozzia  alpina.  ./.?. 
Tracheid-like  cells  in  nucellus,   100, 

109. 
Tradescantia,  81,  135,  136;  virginica, 

63. 

Trapa.  171.  205:  natans,  206. 
Trapella.  55,  80,  85,  95,  106,  110,  111, 

177.  199:  sinensis,  85. 
Tremandiaceae,  247. 
Tretjakow.  >..  217.  218.  221. 
Treub.  M..  40.  50.  59,  61.  64?  66,  71, 

79,  80.  84.  85.  87.  01.  02.   149,  166, 

167.    170.   193.    104.    100.   200,  201, 

212.  213.  21*.  221. 
Treviranus.  213. 
Tricyrtis.    04.    77.    00.    00.    104.    158. 

174:   hirta.  77.  111.  112.  153.  157. 
Trifolium.    pratense,    221;    resupina- 

tum,  203. 


Triglochin,  63,  192;  maritima,  99. 

Trigoniaceae,  247. 

Trillium,  30,  64,  77,  86,  89;  grandi- 

florum,   81,   90,    159;    recurvatum, 

52..  12,  81. 
Triple  fusion,  158,  160,  166;   nature 

of,  182. 

Triplochitonaceae,  249. 
Triticum,  63,  136,  137;  vulgare,  81. 
Tritonia,  77. 

Triuridaceae,  229,  263,  266. 
Triuridales,  229. 
Trochodendraceae,  245. 
Tropaeolaceae,  247. 
Tropaeolurn,  39,  171,  207. 
Trophophylls,  282. 
Tschirch,  A.,  106. 
Tschistiakoff,  I..  125. 
Tube    nucleus,    133;    fragmentation 

of,  135. 

Tubiflorae,  256. 
Tubiflorales,  256,  269. 
Tulasne,  L.  R.,  106. 
Tulipa,    77,    89,    156,    193:    Celsiana, 

156;  Gesneriana,  81,  215,  219,  222; 

sylvestris,  90,  156. 
Tumboa,  310. 
Turneraceae,  249. 
Tussilago,  101. 
Typha,  28,  38,  63,  74,  77,  104,   121, 

131,    133,    229,    233;    latifolia,    28, 

126. 
Typhaceae,  97,  228,  262,  265,  275. 

Ulmaceae,  243. 

Ulmus.  147,  148.  150,  151;  montana, 

150:  pedunculata.  150. 
Umbellales.  251. 
Umbelliferae,   15.   16,  55,  65,  79,  97, 

251.  207. 

Umbelliflorae.  251. 
Unger,  D.  F..  55. 
Urticaceae.  56,  243. 
Urticales.  243. 
Utricularia.  206. 
Utriculariaceae,  106. 
Uvularia,  84. 

Vacciniaceae,  176,  177. 

Vaccinium.  80;  Oxycoccus.  !\2;  ulig- 

ino>um.  ./?. 
Vaillantia,    104,    111;    hispida,    102, 


348 


MORPHOLOGY   OF  ANGIOSPERMS 


Valerianaceae,  18,  259,  269. 

Van  Tieghem,  Ph.,  30,  49,  52,  92, 
297,  298,  309. 

Vascular  bundles,  Monocotyledons 
and  Dicotyledons  contrasted,  4. 

Vegetative,  apogamy,  210;  fertiliza- 
tion, 182;  nucleus,  132. 

Velloziaceae,  236,  264,  266. 

Verbenaceae,  80,  176,  177,  256,  269. 

Verticillatae,  242. 

Vesque,  J.,  63,  65,  71,  77,  80,  84,  85, 
86. 

Viburnum,  277,  278. 

Vicia  narbonnensis,  204. 

Vinca,  136. 

Vincetoxicum,  medium,  221;  nig- 
rurn,  217,  221. 

Viola,  25. 

Violaceae,  249. 

Viscum,  61,  97,  176,  206;  album, 
221;  articulatum,  79,  87. 

Vitaceae,  249. 

Viticella,  156. 

Vochysiaceae,  247. 

Ward,  H.  Marshall,  58,  61,  63,  71, 
76,  77,  80,  87,  92,  94,  148,  194. 

Warming,  E.,  28,  32,  33,  51,  52,  53, 
71. 

Webb,  J.  E.,  19,  37,  39,  58,  59,  87, 
108. 


Webber,  H.  J.,  180,  181. 
Weber,  M.,  Fig.  110. 
Westermaier,  M.,  98,  99,  111. 
Wiegand,  K.  M.,  33,  62,  63,  64,  73, 

77,  78,  81,  133,  136,  192. 
Wille,    X.,    121,    123,    124,    125,    126, 

129,  196. 

Williamson,  W.,  301,  302,  Fig.  110. 
Wimmel,  Th.,  125. 
Wolffia,  234. 

Worsdell,  W.  C.,  303,  306,  308,  309. 
Wylie,  R.  B.,  157,  170. 

Xenia,  179. 

Xyridaceae,  56,  235,  264,  266. 

Yucca,    63,    64,    77,    285;     gloriosa, 
84. 

Zamia,  305,  307;  floridana,  304,  Fig. 

111. 
Zannichellia,  27,  28,  46,  51,  192,  196, 

285;  palustris,  195. 
Zea,  94,  98,  153,  157,  158.  172.  179. 
Zingiberaceae,  171,  237,  264,  266. 
Zinger,  X.,  56,  148,  150. 
Zizania,  315. 
Zostera,  37,  74,  77,  122:  marina,  36, 

81,  124. 

Zygomorphy,  15,  16. 
Zygophyllaceae,  20,  247. 


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